The Ventrodorsal Stream Action In Space And Space Perception

The cortical circuit formed by area F4, which occupies the posterior sector of the ventral premotor cortex of the macaque monkey, and area VIP (Colby et al., 1993), which occupies the fundus of the intraparietal sulcus, is involved in the organization of head and arm actions in space. Single neuron studies showed that in area VIP there are two main classes of neurons responding to sensory stimuli: purely visual neurons and bimodal,

Figure 17-2. A. The inferior parietal lobule: monkey-human homology. Lateral view of the macaque monkey brain showing the cytoarchitectonic parcellation of the superior and inferior parietal lobules according to Von Bonin and Bailey (1947). B. Lateral view of the human brain showing the cytoarchitectonic parcellation of the superior and inferior parietal lobules according to Von Economo (1929).

visual and tactile neurons (Colby et al., 1993). Bimodal VIP neurons respond independently to both visual and tactile stimuli. Tactile receptive fields are located predominantly on the face. Tactile and visual receptive fields are usually in "register," that is, the visual receptive field encompasses a three-dimensional spatial region (peri-personal space) around the tactile receptive field. Some bimodal neurons are activated preferentially or even exclusively when 3D objects are moved towards or away from the tactile receptive field. About thirty percent of VIP neurons code space in reference to the monkey's body. There are also neurons that have hybrid receptive fields. These receptive fields change position when the eyes move along a certain axis, but remain fixed when the eyes move along another axis (Duhamel et al., 1997).

Consistent with the single neuron data, are the results of lesion studies (Duhamel, personal communication). Selective electrolytic lesion of area VIP in monkeys determines mild but consistent contralesional neglect for peri-personal space. No changes were observed in ocular saccades, pursuit and optokinetic nystagmus. Tactile stimuli applied to the contralesional side of the face also failed to elicit orienting responses.

Single neurons studies showed that most F4 neurons discharge in association with monkey's active movements (Gentilucci et al., 1988). The movements more represented are head and arm movements, such as head turns and reaching. Most F4 neurons respond to sensory stimuli. As neurons in VIP, F4 sensory-driven neurons can be subdivided into two classes: unimodal, purely sensory neurons, and bimodal, somatosensory and visual neurons (Gentilucci et al., 1988; Fogassi et al., 1992, 1996). Tactile receptive fields, typically large, are located on the face, chest, arm and hand. Visual receptive fields are also large. They are located in register with the tactile ones, and similarly to VIP, confined to the peri-personal space (Gentilucci et al., 1983, 1988; Fogassi et al., 1992, 1996; Graziano et al., 1994). Recently, trimodal neurons responding also to auditory stimuli were described in F4 (Graziano et al., 1999).

Several electrophysiological studies have shown that in most F4 neurons visual receptive fields do not change position with respect to the observer's body when the eyes move (Gentilucci et al., 1983; Fogassi et al., 1992, 1996; Graziano et al., 1994). The visual responses of F4 neurons do not signal positions on the retina, but positions in space relative to the observer. The spatial coordinates of the visual receptive fields are anchored to different body parts, and not to a single reference point, and they are coded in egocentric coordinates (Fogassi et al., 1996a, 1996b). Furthermore, visual receptive fields located around a certain body part (e.g., the arm) move when that body part is moved (Graziano et al., 1997).

Empirical evidence in favor of the simulation-based motor nature of space coding derives from the properties of F4 neurons. In principle there are two main possibilities on what these neurons code. The first is that they code space "visually". If this is so, given a reference point the neurons should signal the location of objects by using a Cartesian or some other geometrical system. The alternative possibility is that the discharge of neurons reflects a potential, simulated motor action directed towards a particular spatial location. This simulated potential action would create a motor space. When a visual stimulus is presented, it evokes directly the simulation of the congruent motor schema which, regardless of whether the action is executed or not, maps the stimulus position in motor terms.

Arguments in favor of the visual hypothesis are the tight temporal link between stimulus presentation and the onset of neural discharge, the response constancy, and the presence of what appears to be a visual receptive field. If, however, there is a strict association between motor actions and stimuli that elicit them, it is not surprising that stimulus presentation determines the effects just described. More direct evidence in favor of a motor space came from the study of properties of F4 neurons in response to moving stimuli. According to the visual hypothesis, each set of neurons, when activated should specify the object location in space, regardless of the stimulation's temporal dimension. A locus 15 cm from the tactile origin of the visual receptive field should remain 15 cm from it regardless of how the object reaches this position. The spatial map, as expressed by receptive field organization, should be basically static. In contrast, in the case of motor space, because time is inherent to movement, the spatial map may have dynamic properties and may vary according to the change in time of the object's spatial location. The experiments of Fogassi et al. (1996) showed that this is indeed the case. The visual receptive field extension of F4 neurons increases in depth when the speed of an approaching stimulus increases.

The notion that spatial awareness is linked to movement is pretty old. Von Helmoltz (1896) proposed the notion that the "a-priori" nature of our representation of space depends on the fact that it is generated by active exploratory behavior. Indeed, as it has been argued elsewhere (see Rizzolatti et al., 1997), a strong support to the notion that spatial awareness derives from motor activity is the demonstration of the existence of peri-personal space. From a purely sensory point of view, there is no principled reason why our eyes should select light stimuli coming exclusively from a space sector located around our body. Light stimuli arriving from far or from near should be equally effective. However, if we consider that peri-personal stimuli occupy the space where the targets of the actions performed by hands and mouth are mostly located, it becomes clear why space is mapped in motor terms.

It is interesting to note the closeness of the view emerging from singleneuron recordings, and the philosophical perspective offered by phenomenological philosophers on space perception (see also Zahavi, 2002). As Merleau-Ponty (1962, p. 243) wrote, space is "...not a sort of ether in which all things float The points in space mark, in our vicinity, the varying range of our aims and our gestures." Furthermore, it is interesting to note that Husserl wrote that every thing we see, we simultaneously also see it as a tactile object, as something which is directly related to the lived body, but not by virtue of its visibility (Husserl, 1989). The body entertains a dual reality of spatial externality and internal subjectivity. The perspectival spatial location of our body provides the essential foundation to our determination of reality. But in contrast to what Husserl considered the physiological definition of the body - by considering it a material object -contemporary neurophysiological research suggests that a part of the body, the sensory-motor system, is also responsible for the phenomenal awareness of the body's relations with the world.

Why is action important in spatial awareness? Because what integrates multiple sensory modalities within the F4-VIP neural circuit is action embodied simulation (Gallese, 2005a, 2005b, 2006). Vision, sound and action are parts of an integrated system; the sight of an object at a given location, or the sound it produces, automatically triggers a "plan" for a specific action directed toward that location. What is a "plan" to act? It is a simulated potential action.

The characterization so far provided of this cortical network would seem at first sight to be fully consistent with the control of body actions within peri-personal space. If, however, we consider the results of lesion of this network, a different picture emerges. Unilateral lesion of the ventral premotor cortex of the monkey, including area F4, produces two series of deficits: motor deficits and perceptual deficits (Rizzolatti et al., 1983; see also Rizzolatti et al., 2001). Motor deficits consist in a reluctance to use the contralesional arm, spontaneously or in response to tactile and visual stimuli, and in a failure to grasp with the mouth food presented contralateral to the side of the lesion. Perceptual deficits concern neglect of the contralesional peripersonal space, and of the personal (tactile) space. A piece of food moved in the contralesional space around the monkey's mouth does not elicit any behavioral reaction. Similarly, when the monkey is fixating a central stimulus, the introduction of food contralateral to the lesion is ignored. In contrast, stimuli presented outside the animal's reach (far space) are immediately detected.

Neglect in humans occurs after lesion of the IPL and, less frequently, following damage of the frontal lobe, and in particular following lesions of area 6, 8, and 45 (see Bisiach and Vallar, 2000). The most severe neglect in humans occurs after lesion of the right IPL. In the full-fledged unilateral neglect, patients may show a more or less complete deviation of the head and eyes towards the ipsilesional side. Routine neurological examination shows that patients with unilateral neglect typically fail to respond to visual stimuli presented in the contralesional half field and to tactile stimuli delivered to the contralesional limbs. As in monkeys, also in humans neglect may selectively affect the extrapersonal and the peripersonal space. In humans, this dissociation was first described by Halligan and Marshall (1991). They examined a patient with severe neglect using a line bisection task. In this task the subject is usually required to mark the midpoint of a series of lines scattered all over a sheet of paper. The task was executed in the near space and in the space beyond hand reaching distance using a laser pen that the patient held in his right hand. The results showed that when the line was bisected in the near space the midpoint mark was displaced to the right, as typically occurs in neglect patients. However, the neglect dramatically improved or even disappeared when the testing was carried out in the far space. A similar dissociation was reported by Berti and Frassinetti (2000). Other authors described the opposite dissociation: severe deficits in tasks carried out in the extrapersonal space, slight or no deficit for tasks performed in the peripersonal space (see Shelton et al., 1990; Cowey et al., 1994, 1999). The lesions causing neglect in humans are usually very large, thus while the findings of separate systems for peripersonal and extrapersonal space are robust and convincing, any precise localization of the two systems in humans is at the moment impossible.

In conclusion, lesions of IPL and its frontal targets both in monkeys and humans determine body awareness deficits. Furthermore, it must be stressed that not only does IPL appear to play a fundamental role in body and spatial awareness, but it is also necessary for the awareness of the quality of objects presented within peripersonal space. Evidence in favor of this point of view comes from a series of clinical and neuropsychological studies. Marshall and Halligan (1988) reported the case of a lady who, due to a severe visual neglect, explicitly denied any difference between the drawing of an intact house and that of the same house when burning, if the relevant features for the discrimination were on the neglected side. However, when forced to choose the house where she would prefer to live, she consistently choose the intact one, showing in this way an implicit knowledge of the content she was unable to report. Berti and Rizzolatti (1992) confirmed these findings in a systematic way. In their experiments patients with severe unilateral neglect were asked to respond as fast as possible to target stimuli presented within the intact visual field by pressing one of two keys according to the category of the target (fruits and animals). Before showing these stimuli, pictures of animals and fruits were presented to the neglected field as priming stimuli.

The patients denied of seeing these priming stimuli. Yet, their responses to the stimuli shown in the intact field were facilitated by the primes. This occurred not only in "highly congruent conditions", that is when the prime stimulus and the target were physically identical (e.g. a dog), but also when prime and stimulus constituted two elements of the same semantic category, though physically dissimilar (e.g. a dog and an elephant).

These findings demonstrate that neglect patients are able to process stimuli presented within the neglected field up to a categorical semantic level of representation. However, they are not aware of them in the absence of IPL processing. This implies that the parieto-premotor circuits of the ventro-dorsal stream must be intact for achieving awareness even of those stimuli, such as fruits or animals that are mostly analyzed in the ventral stream.

Lesions of sensory-motor circuits, whose primary function is that of controlling movements of the body or of body parts towards or away from objects, produce deficits that do not exclusively concern the capacity to orient towards objects or to act upon them. These lesions produce also deficits in body, space, and object awareness.

0 0

Post a comment