Perception Of Extrapersonal Space Research Paper

1. Psychological Aspects

1.1 Basic Processes

Spatial perception involves not one but many specific abilities. Within the visual domain these include locating points in space, determining the orientation of lines and objects, assessing location in depth, appreciating geometric relations between objects, and processing motion, including motion in depth. These spatial skills can be applied to imagined objects as well as to external stimuli, as in the classic experiments of Shepard and Cooper (1986) on mental rotation. These experiments showed that observers take longer to determine whether two objects are identical when the degree of mental rotation needed to align them increases. Similar sets of basic processes contribute to spatial representation in the auditory and somatosensory domains.

1.2 Space Is Represented In Multiple Frameworks

Our subjective experience strongly suggests that we have direct access to a single coherent and overarching representation of space. Whether we localize a stimulus by sight, smell, hearing, or touch, we can respond to it with equal ease and with any motor system at our command. This introspection is misleading. There is no evidence for the existence of a single, explicit, topographic representation of space suitable for incorporating every kind of sensory input and generating every kind of motor output. On the contrary, the evidence points to multiple representations of space, in a variety of coordinate frames, and linked to separate output systems designed to guide specific motor effectors.

The particular representation of space in use at any time depends on the task the subject is trying to perform. For example, if you were to draw out a route for a hiking trip on a map, the route would be in the coordinates of the map, the piece of paper. If you were then going to walk along that route, you would have to begin by locating your current position within that coordinate frame and constructing a representation of the route with respect to your starting point. The first, map-based representation is an example of an allocentric representation, in which locations are represented in reference frames extrinsic to the observer. Allocentric representations include those centered on an object of interest (object-centered) and those in environmental (room-centered or world-centered) coordinates. The second representation, the one in the coordinates of the hiker’s current position, is an example of an egocentric representation, in which locations are represented relative to the observer. Egocentric representations include those in eye-centered, head-centered, hand-centered, and bodycentered coordinates. Experimental work in humans indicates that multiple reference frames can be activated simultaneously (Carlson-Radvansky and Irwin 1994).

2. Neural Aspects

2.1 Impairments Of Spatial Perception In Humans

Much of our knowledge about the neural basis of spatial perception comes from observations in patients with spatial deficits following brain damage. These include a wide range of perceptual and motor deficits, such as poor localization of visual, auditory, or tactile stimuli; inability to determine visual or tactile line orientation; impaired performance on mazes; impairment on tests of mental spatial transformations; right—left confusion; poor drawing; impaired eye movements to points in space; misreaching; defective locomotion in space; and amnesia for routes and locations. As can be seen from this partial list, spatial behavior involves many kinds of skills and, not surprisingly, a number of brain regions have been implicated in spatial perception and performance. Broadly speaking, the parietal lobe is responsible for spatial perception and representation of immediate extrapersonal space, while temporal and parahippocampal cortices are more involved in topographic memory and navigation. The frontal lobe receives input from both parietal and temporal cortex and is responsible for generating actions.

An important point about deficits in spatial perception is that they are far more common after right hemisphere damage than left. While patients with left hemisphere damage may also exhibit spatial deficits, it is clear that the right hemisphere in humans has a superordinate role in spatial processing and behavior (Heilman et al. 1985). Two kinds of spatial deficits following brain damage are particularly illuminating. First, a common sensorimotor deficit following parietal lobe damage is difficulty in using visual information to guide arm movements, referred to as optic ataxia. Patients with optic ataxia have difficulty with everyday tasks that require accurate reaching under visual guidance, such as using a knife and fork. They both misdirect the hand and misorient it with respect to the object, and are most impaired when using the contralesional hand to reach for an object in the contralesional half of space.

A second, classic disorder of spatial perception in humans is the tendency to ignore one half of space, called hemispatial neglect. The most common form of neglect arises from damage to the right parietal lobe and is manifested as a failure to detect objects in the left half of space. Neglect is more than just a visual deficit, however. It can occur separately or jointly across many sensory modalities (Barbieri and De Renzi 1989). Moreover, neglect occurs with respect to many different spatial reference frames. A patient with right parietal lobe damage typically neglects objects on the left but left may be defined with respect to the body, or the line of sight, or with respect to an attended object. Further, this neglect is dynamic, changing from moment to moment with changes in body posture and task demands (Behrmann 2000). Neglect is apparent even in the purely conceptual realm of internal images. Patients exhibit neglect when asked to imagine a familiar scene, such as a city square, and describe the buildings in it. The portion of space that is neglected changes when they are asked to imagine the scene from a different viewpoint (Bisiach and Luzzatti 1978). As this example illustrates, neglect can occur with respect to an internal image constructed by the individual. Patients with neglect show evidence of using multiple reference frames, just as intact individuals do.

2.2 Spatial Perception In Animals Is Impaired By Parietal Cortex Lesions

The role of parietal cortex in spatial perception has been explicitly tested in animal studies. Monkeys with posterior parietal lobe lesions exhibit many of the same deficits seen in humans, including deficits in the appreciation of spatial relations between objects and impairments in eye movements and reaching. They perform normally on tests of object discrimination but are selectively impaired on a spatial task that requires them to judge which of two identical objects is closer to a visual landmark. In contrast, monkeys with temporal lobe lesions are unimpaired on the spatial task but fail to discriminate between or recognize objects (Ungerleider and Mishkin 1982). This double dissociation between the effects of lesions, in combination with the discovery of distinctive cortical inputs to the parietal and temporal lobes, led to the concept of the dorsal and ventral visual processing streams.

Neurons in the dorsal stream encode the types of visual information necessary for spatial perception. Neurons in specific dorsal stream areas are selective for orientation, depth, direction and speed of motion, rotation, and many other stimulus qualities appropriate for perceiving spatial information. The dorsal visual processing stream leads to posterior parietal cortex, where many kinds of visual information converge, including information about stimulus shape. An equivalent set of somatosensory processing areas send tactile information to anterior parietal cortex. Visual and somatosensory signals converge on single neurons within the intraparietal sulcus, which divides anterior and posterior parietal cortex. Auditory signals have also been demonstrated to contribute to spatial processing in monkey parietal cortex.

2.3 Parietal Neurons Encode Spatial Information In Multiple Reference Frames

The standard approach for investigating the role of parietal neurons in spatial perception is to record electrical activity from individual neurons while the monkey performs a spatial task. Because brain tissue itself has no sensory receptors, fine microelectrodes can be introduced into the brain without disturbing the animal’s performance. By recording neural responses during carefully designed tasks, neural activity can be related directly to the sensory and representational processes that underlie spatial behavior. The general conclusion from these studies is that the function of parietal cortex is to transform spatial information from sensory coordinates into the motor coordinates that are necessary for the guidance of action (Stein 1992, Andersen et al. 1997, Colby and Goldberg 1999).

2.3.1 Head-Centered Spatial Representation In The Ventral Intraparietal Area (VIP). Area VIP is located in the floor of the intraparietal sulcus, where inputs from high-order visual and somatosensory cortex converge. In the visual domain, VIP neurons are characterized by direction and speed selectivity, and thus resemble neurons in other dorsal stream visual areas that process stimulus motion. In the somatosensory domain, these same neurons respond to light touch on the head and face. The somatosensory and visual receptive fields of individual neurons exhibit strong spatial correspondence: they match in location, in size, and even in their preferred direction of motion. The existence of spatially matched receptive fields raises an interesting question: what happens when the eyes move away from primary position? If the visual receptive fields were simply retinotopic, they would have to move in space when the eyes do and so would no longer match the location of the somatosensory receptive field. Instead, for some VIP neurons, the visual receptive field moves to a new location on the retina when the eyes move away from the straightahead position. For example, a neuron that has a somatosensory receptive field near the mouth and responds best to a visual stimulus moving toward the mouth will continue to respond to that trajectory of motion regardless of where the monkey is looking (Colby et al. 1993). These neurons have head-centered receptive fields: they respond to stimulation of a certain portion of the skin surface and to the visual stimulus aligned with it, no matter what part of the retina is activated. Neurons in area VIP send projections to the region of premotor cortex (see Sect. 2.4.1) that generates head movements. Area VIP neurons thus contribute to the visual guidance of head movements and may play a special role in hand, eye, and mouth coordination. They operate in a head-centered reference frame in order to generate appropriate signals for a particular motor effector system, namely that which controls head movements.

2.3.2 Eye-Centered Spatial Representation In The Lateral Intraparietal Area (LIP). In contrast to area VIP, neurons in area LIP construct an eye-centered spatial representation. Individual neurons become active when a salient event occurs at the location of the receptive field. This can be a sensory event, such as the onset of a visual or auditory stimulus, or a motor event, such as a saccade towards the receptive field, or even a cognitive event, such as the expectation that a stimulus is about to appear, or the memory that one has recently appeared. The level of response reflects the degree to which attention has been allocated to the site of the receptive field (Colby et al. 1995).

Again, as we saw for area VIP, the animal’s ability to make eye movements raises an interesting question about spatial representation. Neural representations of space are maintained over time, and the brain must solve the problem of how to update these representations when a receptor surface moves. With each eye movement, every object in our surroundings activates a new set of retinal neurons. Despite this constant change, we perceive the world as stable. Area LIP neurons contribute to this perceptual stability by using information about the metrics of the eye movement to update their spatial representation of salient locations (Duhamel et al. 1992). For example, LIP neurons are activated when the monkey makes an eye movement that brings a previously illuminated screen location into their receptive field. These neurons respond to the memory trace of the earlier stimulus: no stimulus is ever physically present in the receptive field, either before or after the saccade. The proposed explanation for this surprising finding is that the memory trace of the stimulus is updated at the time of the saccade. Before the saccade, while the monkey is looking straight ahead, the onset of the stimulus activates a set of LIP neurons whose receptive fields encompass the stimulated screen location, and they continue to respond after the stimulus is extinguished, maintaining a memory trace of the stimulus. At the time of the saccade, a corollary discharge, or copy of the eye movement command, containing information about the metrics of the saccade, arrives in parietal cortex. This corollary discharge causes the active LIP neurons to transmit their signals to the new set of LIP neurons whose receptive fields will encompass the stimulated screen location after the saccade. The representation of the stimulated location is thus dynamically updated from the coordinates of the initial eye position to the coordinates of the final eye position.

The significance of this observation is in what it reveals about spatial representation in area LIP. It demonstrates that the representation is dynamic and is always centered on the current position of the fovea. Instead of creating a spatial representation that is in purely retinotopic (sensory) coordinates, tied exclusively to the specific neurons initially activated by the stimulus, area LIP constructs a representation in eye- centered (motor) coordinates. The distinction is a subtle one but critical for the ability to generate accurate spatial behavior. By representing visual information in eye-centered coordinates, area LIP neurons tell the monkey not just where the stimulus was on the retina when it first appeared but also where it would be now if it were still visible. The result is that the monkey always has accurate spatial information with which to program an eye movement toward a real or remembered target. The transformation from sensory to motor coordinates puts the visual information in its most immediately useful form. Compared to a head-centered or world-centered representation, an eye-centered representation has the significant advantage that it is already in the coordinates of the effector system that will be used to acquire the target. Humans with unilateral parietal lobe damage fail on an eye movement task that requires an eye-centered representation of a remembered target position. This failure presumably reflects an impairment of the updating mechanism in parietal cortex.

In sum, posterior parietal cortex plays a critical role in spatial perception and representation (Colby and Goldberg 1999). Physiological studies in monkeys show that parietal neurons represent spatial locations relative to multiple reference frames, including those centered on the head and the eye. Individual neurons (in area VIP) combine spatial information across different sensory modalities, and specific spatial reference frames are constructed by combining sensory and motor signals (in area LIP). In accord with the physiology, human neuropsychological studies show that neglect can be expressed with respect to several different reference frames.

2.4 Frontal Lobe Mechanisms Of Spatial Representation

The parietal lobe transforms sensory representations of attended objects into the motor coordinate frames most appropriate for action. They do not actually generate those actions. Dorsal stream outputs to frontal cortex provide the sensory basis, in the correct spatial framework, for producing specific motor outputs. The following sections describe specific spatial representations found in three regions of frontal cortex.

2.4.1 Neurons In Premotor Cortex Have Head-Centered And Hand-Centered Visual Receptive fields. Two different forms of spatially organized visual responsiveness have been described in ventral premotor cortex. First, in subdivisions representing facial movements, neurons respond to visual stimuli at specific locations relative to the head, much like those described above in area VIP. These neurons have been characterized by recording activity while objects approach the monkey’s head along various trajectories. The preferred trajectory is constant with respect to the head, and is not affected by changes in eye position (Fogassi et al. 1996). This specific zone of premotor cortex receives inputs from area VIP, and uses the same form of spatial representation. In both cases, stimuli are represented in the motor coordinate frame that would be most useful for acquiring or avoiding stimuli near the face by means of a head movement.

A different kind of spatial representation has been observed in subdivisions of premotor cortex involved in generating arm movements. Here, neurons respond to visual stimuli presented in the vicinity of the hand. When the hand moves to a new location, the visual receptive field moves with it. Moreover, the visual receptive field remains fixed to the hand regardless of where the monkey is looking, suggesting the existence of a hand-centered representation (Graziano et al. 1994). A fascinating observation indicates that some neurons in this area are capable of even more abstract forms of representation. Rizzolatti and coworkers have described neurons in premotor cortex that are activated both when the monkey grasps an object, such as a raisin, and when the monkey observes the experimenter performing the same action (Gallese et al. 1996). These ‘mirror’ neurons encode not just the monkey’s own motor actions but also the meaning of actions performed by others.

2.4.2 Object-Centered Spatial Representation In The Supplementary Eye field (SEF). Actions are directed toward objects in the environment and toward specific locations on an object. Picking up your coffee cup requires that you locate both the cup in egocentric space and the handle in relation to the cup. The spatial reference frame that guides such movements is not limited to the egocentric representations described above. Evidence from the supplementary eye field (SEF) demonstrates that single neurons can encode movement direction relative to the object itself (Olson and Gettner 1995). The SEF is a division of premotor cortex with attentional and oculomotor functions. Neurons here fire before and during saccades. In monkeys trained to make eye movements to particular locations on an object, SEF neurons exhibit a unique form of spatial selectivity: they encode the direction of the impending eye movement as defined relative to an object-centered reference frame. For example, a given neuron may fire when the monkey looks toward the right end of a bar placed at any of several different locations on the screen, regardless of whether the eye movement itself is a rightward or leftward saccade. Moreover, the same neuron will fail to respond when the monkey makes a physically identical eye movement toward the left end of the bar stimulus. This striking result indicates that single neurons can make use of quite abstract spatial reference frames. Object-centered spatial information could potentially guide arm movements as well as eye movements. Moreover, neuropsychological evidence indicates that an object-centered reference frame can be used to direct attention: some patients exhibit object-centered neglect after parietal lobe damage (Behrmann 2000). Parietal lobe lesions in monkeys likewise produce impairments on tasks that require an object-centered spatial representation.

In sum, behavioral and neuropsychological studies indicate that we make use of multiple spatial representations in the perception of extrapersonal space. Neurophysiological studies are beginning to uncover the neural mechanisms underlying the construction of these egocentric and allocentric spatial representations.

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