From Towards a Science of Consciousness Section 4: Vision and Consciousness -- Introduction CogNet Proceedings
There are many different ways to approach the study of brain functions. The data that will be reported here have been acquired by using a "naturalistic" approach. What does it mean? A naturalistic approach, when applied to neurophysiology, consists in choosing the most appropriate way of testing neurons activity, by figuring out what would be the stimuli or the behavioral situation that more closely approximate what the animal we are recording from would experience in its natural environment. The "answers" we are seeking from neuronal activity are strongly influenced by the way in which we pose our "questions." Too many experimental data are collected by routinely applying behavioral paradigms good for all purposes. Another flaw commonly encountered in part of the contemporary neurophysiological literature is the poor, if any, attention paid to investigate where from is recorded what. Altogether, these factors have induced among many scholars of this discipline a growing sense of discomfort with the single neuron recording approach.
My point, as neurophysiologist, is that the single neuron recording approach still represents a very powerful and creative tool to unravel the neural correlates of many cognitive functions. This goal can be achieved provided that we are able to broaden the theoretical background in which the experimental data are to be framed, by integrating the findings and the contributions coming from other disciplines such as psychology, cognitive ethology, and philosophy.
In the following sections I will expose results which are in line with the theoretical and methodological principles that I have only briefly sketched above. I will show how some of the visuo-motor processes occurring in the macaque monkey premotor cortex may provide new insights on issues such as action understanding and the origin of language.
This approach led during the last two decades to the discovery of the existence of multiple cortical representations of hand movements in the inferior parietal lobule and in the ventral premotor cortex (Hyvärinen and Poranen 1974, Mountcastle et al. 1975, Rizzolatti et al. 1981, Rizzolatti 1987, Gentilucci et al. 1988, Rizzolatti et al. 1988, Sakata et al. 1995). The anticipatory discharge with respect to movement onset of many neurons of these areas lead to hypothesize for them an important role in the planning of movements.
I will focus my attention on the premotor cortex, the cortex that lies rostral to the primary motor cortex. Converging anatomical evidence (see Matelli and Luppino 1997) supports the notion that the ventral premotor cortex (referred to also as inferior area 6) is composed of two distinct areas, designated as F4 and F5 (Matelli et al. 1985). As shown in figure 15.1, area F5 occupies the rostralmost part of inferior area 6, extending rostrally within the posterior bank of the inferior limb of the arcuate sulcus. Area F5 is reciprocally connected with the hand field of the primary motor cortex (Matelli et al. 1986) and has direct, although limited, projections to the upper cervical segments of the spinal chord (He et al. 1993). Intracortical microstimulation evokes in F5 hand and mouth movements at thresholds generally higher than in the primary motor cortex (Gentilucci et al. 1988, Hepp-Reymond et al. 1994). The functional properties of F5 neurons were assessed in a series of single unit recording experiments (Rizzolatti et al. 1981, Okano and Tanji 1987, Rizzolatti et al. 1988). These experiments showed that the activity of F5 neurons is correlated with specific distal motor acts and not with the execution of individual movements. What makes of a movement a motor act is the presence of a goal. Using the effective motor act as the classification criterion, the following types of neurons were described: "Grasping neurons," "Holding neurons," "Tearing neurons," and "Manipulation neurons." Let us concentrate on the first class: grasping neurons discharge when the monkey performs movements aimed to take possession of objects with the hand ("Grasping-with the-hand neurons"), with the mouth ("Grasping-with-the-mouth neurons"), or with both ("Grasping-with-the-hand-and-the-mouth neurons"). Grasping-with-the-hand neurons form the largest class of F5 neurons. Most neurons of this class are selective for different types of grip. By observing the way in which the monkey grasped objects, three basic types of hand prehension were distinguished: precision grip (opposition of the pulpar surface of the index finger and thumb) normally used to grasp small objects, finger prehension (opposition of the thumb to the other fingers) used to grasp middle-size objects and whole hand prehension (flexion of all fingers around an object) used to grasp large objects. The majority of F5 grasping neurons is selective for precision grip.
The most interesting aspect of F5 neurons is that they code movement in quite abstract terms. What is coded is not simply a parameter such as force or movement direction, but rather the relationship, in motor terms, between the agent and the obiect of the action. F5 neurons become active only if a particular type of action (e.g., grasp, hold, etc.) is executed to achieve a particular type of goal (e.g., to take possession of a piece of food, to throw away an object, etc.). The metaphor of a "motor vocabulary" has been introduced (Rizzolatti and Gentilucci 1988) in order to conceptualize the function of these neurons. The presence in the motor system of a "vocabulary" of motor acts allows a much simpler selection of a particular action within a given context. Either when the action is self-generated or externally generated, only a few "words" need to be selected. Let us imagine that a monkey is presented with a small object, say a raisin, within its reaching distance. If the motivational value of the stimulus is powerful enough to trigger an appetitive behavior, it will evoke a command for a grasping action; then the command will address a specific finger configuration, suitable to grasp the raisin in that particular context. Within the context of a motor "vocabulary," motor action can be conceived as a simple assembly of words, instead of being described in the less economical terms of the control of individual movements.
Since most grasping actions are executed under visual guidance, it is extremely interesting to elucidate the relationship between the features of 3D visual objects and the specific words of the motor vocabulary. According to this logic, the appearance of a graspable object in the visual space will retrieve immediately the appropriate ensemble of words. This process, in neurophysiological terms, implies that the same neuron must be able not only to code motor acts, but also to respond to the visual features triggering them. About twenty percent of F5 grasping neurons, when clinically tested, indeed responded to the visual presentation of objects of different size in absence of any detectable movement (Rizzolatti et al. 1988). Very often a strict congruence was observed between the type of grip coded by a given neuron and the size of the object effective in triggering its visual response. These neurons, which match the "intrinsic" object properties with the most appropriate type of prehension, appear to be good candidates to perform the process of visuo-motor transformation. It was during the study of the visual properties of grasping neurons that mirror neurons were discovered.
Let us briefly summarize the naturalistic approach when recording mirror neurons from area F5. The awake monkey is confortably seated on a primate chair. Single neuron activity is recorded by means of a microelectrode. Once a neuron is isolated, its visual and motor properties are studied. The monkey is presented with various objects: they consist of food items (raisins, pieces of apple, sunflower seeds) and of objects of different size and shapes. Objects are presented at different locations with respect to the monkey, within and outside its reaching distance. Prehension movements are studied by presenting the same objects used for visual testing, and by letting the monkey grasp them. Everytime a neuron become active during prehension movements its properties are formally tested within a behavioral controlled paradigm in which arm and hand movements of the monkey are recorded, both in light and in darkness, using a computerized movement recording system and subsequently correlated with the recorded neuronal activity.
Mirror properties were studied by performing a series of actions in different spatial locations with respect to the monkey. These actions could be transitive movements (such as grasping, holding, manipulating, or tearing objects) or intransitive movements with or without emotional content (arms lifting, waving hands, threatening gestures, and so on). In order to verify whether the recorded neuron coded specifically hand-objects interactions the following actions were also performed: hand movements mimicking object-related actions in absence of the objects; prehension movements performed by using tools such as pincers or pliers; simultaneous movements of hands and objects kept spatially separated. Finally, in order to rule out the possibility that mirror neurons activation during the observation of hand-object interactions could be due to unspecific factors such as food expectancy or motor preparation for food retrieval or reward, we studied a set of neurons by using a second monkey as action performer, being the recorded monkey with its hands restrained and thus not receiving any reward.
All mirror neurons discharged during specific goal-related motor acts. Grasping, manipulating and holding objects were by far the most effective actions that triggered their motor response. Among them about fifty percent discharged during a specific type of prehension, being precision grip the most represented one. The visual stimuli most effective in triggering mirror neurons visual responses were actions in which the experimenter, or a second monkey, interacted with objects with their hand or with their mouth. Neither the sight of the object alone or of the agent alone were effective in evoking the neuronal response. Similarly, ineffective were mimicking an action without a target object, or performing the action by using tools. In over 90 percent of mirror neurons a clear correlation between the most effective observed action and their motor response was observed. In one third of them this correlation was strict both in terms of the general goal of the action (e.g., grasping) and in terms of the way in which it was executed (e.g., precision grip) (Gallese et al. 1996, Rizzolatti et al. 1996a). Figure 15.2 shows two examples of mirror neurons.
On the basis of their functional properties, here briefly summarized, mirror neurons appear to form a cortical system that matches observation and execution of motor actions. What could be the possible functional role of this matching system? Before addressing this important issue it is important to stress that the existence of such a system has been demonstrated also in humans.
These results posed the question of the anatomical location of the mirror system within the human brain. This issue has been addressed by two brain imaging experiments utilizing the technique of Positron Emission Tomography (PET). These two experiments (Rizzolatti et al. 1996b, Grafton et al. 1996), although different for many aspects, both shared a condition in which normal human subjects observed the experimenter grasping 3D objects. Both studies used the observation of the same objects as control condition. The results showed that grasping observation significantly activates the cortex of the left superior temporal sulcus, of the left inferior parietal lobule and of the anterior part of Broca's region. The activation during action observation of a cortical sector of the human brain traditionally linked with language raises the problem of the possible homologies between Broca's region and the premotor area F5 of the monkey, in which mirror neurons have been discovered. This point will be addressed in the section on the origin of language.
Neurons responding to complex biological stimuli had been previously described in the macaque brain. A series of studies showed that in the inferior temporal cortex there are neurons that discharge selectively to the presentation of faces or hands (Gross et al. 1972, Perrett et al. 1982, Gross et al. 1985). More recently it has been showed that some of these neurons respond to specific features of these stimuli (see Tanaka et al. 1991). Neurons responding to complex biological visual stimuli such as walking, climbing, approaching another individual, were reported also in the amygdala (Brothers et al. 1990). Even more relevant to the present issue is the work of Perrett and coworkers. These authors showed that in the upper bank of the superior temporal sulcus (STS) there are neurons selective to the observation of hand movements (Perrett et al. 1982 1989, 1990). These properties resemble the visual properties of F5 mirror neurons very much: both populations of neurons code the same types of actions; they both generalize their responses to the different instances of the same action; they both are not responsive to mimicked hand actions without the target object. However, the distinctive feature of F5 mirror neurons reside in the fact that they also discharge during active movements of the observer. An observed action produces the same neural pattern of activation as does the action actively made by the observer.
The presence of two brain regions with neurons endowed with similar complex visual properties, raises the question of their possible relationship. Two possibilities might be suggested. One is that F5 mirror neurons and STS neurons have different functional roles. STS neurons would code the semantic, the meaning of hand-object interactions, while F5 mirror neurons would be engaged in the pragmatic coding of the same actions. Being area F5 recipient of visual information fed mainly by the parietal lobe (see Matelli et al. 1986, 1994), this hypothesis is in line with theories positing a sharp distinction between pragmatic and semantic coding within the two main streams of visual processing (see Milner and Goodale 1995).
A second possibility, that I personally favor, is that these two "action detector" systems would represent distinct stages of the same analysis. The STS neurons would provide an initial "pictorial" description of actions that would be then fed, (likely through an intermediate step in the posterior parietal cortex), to the F5 motor vocabulary where it would acquire a meaning for the individual. This latter hypothesis stresses the importance of the motor system in providing meaning to what is "described" by the visual system, by positing a pragmatic "validation" of what is perceived. Experimental evidence so far does not allow to rule out either of the two hypotheses.
What may be the functional role of the mirror matching system? Why has evolution provided individuals with such a mechanism? Mammals are usually engaged in relationships with conspecifics. This social attitude is particularly evident among primates. Macaque monkeys live in groups characterized by several active and intense social interactions, such as grooming (see Dunbar 1993), that are usually disciplined by a well delineated hierarchical organization. It is therefore very important for each member of a given social group to be able to recognize the presence of another individual performing an action, to discriminate the observed action from others, and to "understand" the meaning of the observed action in order to appropiately react to it. Whenever an individual emits an action it is able to predict its consequences. This knowledge is likely built by associating, through learning, the goal of the action, coded in the motor centers, with its consequences as monitored by the sensory systems. The matching system represented by mirror neurons could provide the neuronal basis for such a process of "action understanding," a basic requisite for social communication.
A thorough discussion of this problem, which is a key passage toward the understanding of the distinctiveness of being humans, is beyond the scope of this essay. My main concern here is to suggest that the discovery of mirror neurons may provide a new, although still sketchy, neurobiological basis to account for the emergence of language (see Rizzolatti and Arbib 1998 for a thorough discussion of these points). This assumption is founded on the following premises: a) Language skill has emerged through evolution by means of a process of preadaptation: specific behaviors and the nervous structures supporting them, originally selected for other purposes, acquire new functions that side and eventually supersede the previous one. b) A continuity can be traced between language skill and prelanguage brachio-manual behaviors, being the primate premotor cortex the common playground of this evolutionary continuity; c) The specialization for language of human Broca's region derives from an ancient mechanism, the mirror system, originally devised for action understanding.
After having delimited the theoretical background, let us examine the empirical findings upon which it can be grounded. The finding from brain imaging experiments, reported above, that in humans the observation of hand actions activates the Broca's region, an area classically considered to be mainly involved in speech control, raises queries about a possible homology between Broca's region and monkey area F5, where mirror neurons have been recorded. Once such an homology could be established, the ties between F5 and language could be more firmly asserted.
In monkey, the caudal sector of the ventral part of the frontal lobe (ventral premotor area) is constituted of two areas: area F4 caudally (FB according to Von Bonin and Bailey 1947), and area F5, rostrally (FCBm of Von Bonin and Bailey). Both areas have basically an agranular structure. Area F5 shows a rough somatotopic organization, although with a considerable overlap: hand movements are represented mostly in its rostral part (Rizzolatti 1987, Okano and Tanji 1987, Gentilucci et al. 1988, Rizzolatti et al. 1988, Hepp-Reymond et al. 1994), while face, mouth and larynx movements are mostly laterally represented (Hast et al. 1974, Gentilucci et al. 1988).
The organization of the ventral part of human inferior frontal lobe comprises in its rostral sector two separate areas (areas 44 and 45) differing for some cytoarchitectonical features, although, according to Campbell (1905), both these areas belong to the same "intermediate (premotor) type of cortex." Area 44 and 45 constitute Broca's region. It is generally agreed that, because of its anatomical location and cytoarchitectonic structure, F5 is the most likely homologue of human area 44 (see Petrides and Pandya 1994). Area F5 is a large area with most of its extent buried inside the lower limb of the arcuate sulcus of which it constitutes the posterior bank. A recent cytoarchitectonical study (Matelli et al. 1996) demonstrated that area F5 consists of several sectors. Mirror neurons are clustered in one of them. This dishomogeneity provides a clue for an initial segmentation of F5 into different areas, suggesting that a similar process could have occurred also in humans. It is possible therefore that human area 45 is the homologue of one of the subdivisions of F5.
Broca's region is by definition related to speech. A recent series of data indicate, however, that the two cytoarchitectonic areas forming it contain also a representation of hand movements. Bonda et al. (1994) showed in a PET study that this region becomes active during the execution of self-ordered hand movement sequences. In another PET study, Parsons et al. (1994) demonstrated a marked increase of Broca's region activation during a task in which subjects were required to imagine to rotate their hands. Furthermore, part of Broca's region is activated when subjects perform mental imagery of hand grasping tasks (Decety et al. 1994, Grafton et al. 1996).
The not exclusive role of Broca's region in speech function is supported also by clinical data on aphasic patients. Many of them show, beside language deficits, difficulties in pantomime recognition (Bell 1994). According to this author, the ability to recognize pantomime is represented in Broca's region as a specific language independent function.
The above listed series of anatomical, experimental, and clinical evidence allows one to conclude that area F5 and at least part of Broca's region can be considered homologue. Both areas are endowed with hand and mouth motor representations. The latter expanded enormously in humans in relation to the high demanding requirements of words emission. The hand-related functions, however did not disappear from Broca's region and, as showed by Bell (1994), retained a role in gestures recognition. At first glance it might seem counterintuitive, if not paradoxical, to root the origin of language into a system related to gestures recognition, since language means essentially speech production. It would appear therefore more logical to look for a vocal antecedent. Vocal calls are commonly uttered by nonhuman primates. These vocalizations, however, at difference with human speech, are usually emitted in response to emotionally indexed events, and appear therefore related to instinctual behavior. Furthermore, the anatomical structures responsible of the control of vocal calls emission are represented by the cingulate cortex together with diencephalic and brainstem structures (Jurgens 1987, MacLean 1993). All these considerations could lead one to give up an evolutionary explanation of language (see, however, Pinker and Bloom 1990), and accept the nativist, mentalist definition of language as proposed by Chomsky (1986), who asserts that language capacity cannot be derived from lower species of animals. An alternative solution, however, can be found in the "motor theory of speech perception" proposed by Libermann several years ago (Libermann et al. 1967). According to Libermann's theory the "objects" of speech perception are not the sounds but the phonetic gestures of the speaker. These gestures are represented in the brain as invariant motor commands. As stressed by Libermann and Mattingly (1985) the phonetic gestures are the "primitives that the mechanisms of speech production translate into actual articulatory movements, and they are also the primitives that the specialized mechanisms of speech perception recover from the signal." The similarity of this mechanism with mirror neurons is striking: in both cases at the basis of gesture recognition there is an action/perception matching system. The modality is different, acoustic in the case of speech, visual for mirror neurons. Note, however, that language has not to be necessarily and exclusively assigned to the vocal-auditory domain, but can be exhibited also in the brachio-manual visual domain, as in the case of sign language used by deaf people. In fact, deaf signers suffering from left hemisphere lesions show impairments in their visual-gestural language, such as extreme disfluency and almost exclusive use of referential open-class nouns, that are very similar to the impairments that characterize Broca-like aphasics (see Poizner et al. 1984). These data corroborate the notion that the specialization for language of the left hemisphere of humans is independent of language modality.
My proposal is that this specialization resides in gesture recognition. Broca's region likely became a language area within a process of evolutionary continuity between its homologue precursor area, monkey premotor area F5, which well before language appearance was already endowed with the capacity of recognizing gestures. Mirror neurons are the neuronal basis of this capacity.
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