Some Neurons Encode the Possibilities for Interaction with an Object
The studies of the parietal and premotor canonical neurons led Michael Arbib, and subsequently Rizzolatti and Giuseppe Luppino, to formulate a new model of how sensory representations of objects are transformed into hand movements.
Their model is based on the functional significance of the responses of visual-dominant and visual-and-motor neurons in the anterior intraparietal area to the presentation of three-dimensional objects. Their thinking about these responses was influenced by the notion of affordance introduced several years ago by the psychologist James J. Gibson. According to Gibson the sight of an object triggers an immediate and automatic selection of those properties of the object that allow one to interact with it. These properties, or affordances, are not the visual aspects of the object (shape, mass, color, etc.) but the pragmatic opportunities that the object affords the observer.
As we have seen, aspects of visual stimuli that are useful for action are analyzed in the dorsal stream of the visual system. Based on the extensive elaboration of an object's properties in the extrastriate visual areas of the dorsal stream beginning in V2, the visual-dominant and visual-and-motor neurons in the anterior intraparietal cortex are able to encode the object's affordances. This information is then sent to F5 neurons that encode potential motor acts. An F5 neuron can transform a given affordance into an appropriate potential motor act because of the congruence of its response to the affordance and the motor act it controls. Object becomes action.
In real life objects usually have more than one affordance and may be grasped in several ways. How does the brain determine which is optimal? Behavioral analysis of grasping reveals that nonvisual factors determine the choice of affordance and thus how an object will actually be grasped. These factors relate both to what the object is for and the individual's intent at that moment. A cup is a simple example. The cup has three major affordances: the handle, the top, and the body. If the cup is recognized as a cup and the person wants to use it in the way a cup is commonly used, the person will grasp it by the handle. However, if the person wants to move the cup or give it to someone, the cup may be taken not by the handle but by its body or its rim (Figure 19–8).
Neural control of grasping.
The sight of a cup automatically triggers the motor act appropriate for grasping it. The brain centers involved in grasping are indicated below, and the operations carried out by them are summarized in the upper part of the figure. Affordances are not the visual aspects of the object (shape, size, color, etc.) but the pragmatic opportunities that the object affords the observer. (AIP, anterior intraparietal area; PMv, ventral premotor cortex; IT, inferotemporal cortex.)
Thus a more complete (and realistic) model of the grasping circuit involving the anterior intraparietal area and the premotor area F5 must assume that the circuit extracts automatically not one but all the affordances of an object. A specific affordance will be selected according to the information the circuit receives about the meaning of the object and the individual's intention.
As far as the meaning of the object is concerned, the ventral visual stream (Figure 19–8) is specifically dedicated to description of objects. This stream ends in the inferotemporal lobe, which is richly connected reciprocally with the inferior parietal lobe, including the anterior intraparietal area. It is likely that these connections convey to the parietal lobe the semantic properties of an object; this information, as well as the motor use of the object specified in the premotor circuits, is the basis for the selection of an appropriate affordance consistent with the standard uses of the object.
The anatomical substrate for selecting affordances on the basis of the individual's current goal could be the input to the inferior parietal lobe from the prefrontal lobe, where long-term motor planning occurs. Thus when an unconventional use of an object is intended, the prefrontal input could override the selection of standard affordances and select those affordances that are congruent with the individual's intention. For example, if an individual wants to throw a cup instead of drinking from it, the affordances presented by the body of the cup or its top will be selected rather than the affordance presented by the handle.
Mirror Neurons Respond to the Motor Actions of Others
Canonical neurons discharge both when the monkey acts on an object and when it simply looks at the object without acting. In both cases these neurons fire in much the same manner and send the same signal to other neural centers. The firing of the neuron in the absence of an overt movement represents therefore a potential motor act: This activity occurs in a circuit that plans a movement but does not trigger a motor command. Potential motor acts afford an individual the freedom to choose whether or not to respond to a stimulus or simply hold it in memory.
Potential motor acts have an entirely different significance in a set of extremely interesting visuomotor neurons, the mirror neurons, in area F5. These neurons, like all neurons in F5, discharge during specific motor acts such as grasping, tearing, or holding. In addition, they also fire when the monkey observes another individual (human or monkey) performing the same motor act. They do not discharge in response to mere object presentation. In other words, these neurons represent the action done by another individual as a potential motor act.
What may be the function of these neurons? One attractive idea is that individuals know the outcome of the motor acts they plan. Thus, when the mirror neurons discharge in response to a motor act done by another individual, the observer understands what the other individual is doing because the observed action elicits in his premotor cortex a motor plan whose outcome is known to him.
At first glance it may seem strange that our motor faculties might be involved in understanding what others are doing, what their intentions are. But how else could we obtain this information? Although our visual system provides us with a description of the overt aspects of an action, it does not tell us what the action means, what its purpose is. Mirror neurons could in principle provide us with an experience-based understanding of observed actions, a basis for understanding the intention of others (see Chapter 38).
An essential step in the biological evolution of social cognition is our ability to interact with each other in a meaningful and constructive way. When you and I talk, you not only know the content of your own mind but also have a sense of what I am thinking and how I am reacting. A defect in social cognition may contribute to autism, a serious developmental disorder in which a child's ability to communicate socially is impaired. Normal communication requires, in addition to familiarity with language and the ability to express oneself, certain sensitivity to the thoughts and feelings of the person with whom one is communicating. One of the central features of autism is difficulty in understanding the perspectives, thoughts, ideas, and intentions of another person.
The mirror neurons are probably the most basic system the brain has for understanding others' intentions. Other cortical regions, such as the region near the superior temporal sulcus and some rostral medial cortical areas, also play a role in understanding another's intentions, especially when complex reasoning is required.
Potential Motor Acts Are Suppressed or Released by Motor Planning Centers
The representation of potential motor acts by the nervous system raises a further question. What prevents a potential motor act from being executed? Are there control mechanisms inhibiting or facilitating implementation? Damage to certain premotor cortical areas, or the motor cortex, results in neurological syndromes that strongly suggest that there are such controls. Some of these behavioral disorders include difficulty in initiating movements or making movements that are not consciously intended.
A particularly telling example is the utilization behavior syndrome. Individuals with this syndrome pick up objects in an almost compulsive way. Once they observe an object, they immediately grasp it, even if it belongs to another person or to the doctor examining them. This syndrome may result from impaired restraint of the potential motor acts elicited by objects.
A key feature of voluntary motor behavior is that certain motor acts are executed while others are restrained. Voluntary action depends on sequencing elementary movements to form purposeful action. This ability is the prerequisite for many of our daily actions such as typing, using a computer, playing a musical instrument, and even speech. Karl Lashley called the task of sequencing motor actions the "serial order problem" of motor behavior. The sequence of motor actions is thought to involve parallel computations in multiple cortical areas and subcortical nuclei, including the basal ganglia and the supplementary motor area.
Neurons in the supplementary motor area are involved in the planning, generation, and control of sequential motor actions. Thus, when monkeys were trained to perform different sequences of three simple elemental arm movements—push, pull, and turn—some neurons in the supplementary motor area were active before any movement occurred but only when a specific sequence was planned. For example, a neuron could be active prior to the performance of a pull-turn-push sequence but not before a pull-push-turn sequence. Other neurons were active while a particular movement was performed but only if the movement was preceded or followed by another specific movement.