- Email: [email protected]
Brain representation of object-centered space
165
Brain representation of object-centered space Carl R Olson1 and Sonya N Gettner* Object-centered spatial awareness underlies many important cognitive functions, including reading, which requires registering the locations of letters relative to a word, and pattern recognition, which requires registering the locations of features relative to a whole pattern. Recent studies have elucidated the nature of the brain mechanisms underlying this form of spatial awareness by showing that attention tends to focus on objects rather than on regions of space: by demonstrating that each hemisphere contributes selectively to awareness of the opposite half of object space, and by revealing that neurons in some cortical areas are selective for particular locations in object space. These results are concordant with the general idea that imagining or attending to an object is accompanied by projecting its image onto a neural map of object-centered space. An important aim for future studies will be to test and extend this ‘object map’ hypothesis.
Address Department of Oral and Craniofacial Biological Sciences, Room 5A12, University of Maryland Dental School, 666 West Baltimore Street, Baltimore, Maryland 21201, USA ‘e-mail: colsonQumabnet.ab.umd.edu 2e-mail: [email protected] Abbreviation supplementary eye field SEF
Current Opinion in Neurobiology
1996, 6:165-l
70
0 Current Biology Ltd ISSN 0959-4388
Introduction When we look at or think about an object, we are aware of its structure. We know, for example, that the letter ‘b’ would have to be rotated out of the page in order to transform it into the letter ‘p’. Recent work has indicated that this structural awareness may depend on a neural system with two distinctive traits: first, it contains neurons that are selective for locations as defined relative to a reference frame centered on the object itself, and second, these neurons are arranged so that their spatial fields form a map of object-centered space. The object map can be thought of as a ‘screen’ or ‘visuospatial scratchpad’ on which the image of an object is projected by scaling, translating and rotating it to produce a normalized representation [ 1,2]. The object map hypothesis is consistent with a variety of data from recent experiments in several fields. In this review, we will present findings from psychological studies indicating that attention naturally focuses on objects and on particular locations within objects.
We will then describe studies of brain-injured patients demonstrating that neglect can attach to one half of an object rather than to one half of the body or of external recording space. Finally, we will discuss single-neuron studies showing that neurons in some cortical areas are selective for spatial locations as defined with respect to an object-centered reference frame.
Psychology: showing that attention to objects
attaches
The first step toward forming a mental representation of an object is to attend to it. Attention is specifically object based, rather than space based, in the sense that at any given moment it tends to focus on elements that belong to one object, excluding even overlapping or interspersed elements that are not part of that object [3-S]. Recent experiments have strengthened the view that attention is object based by showing that attention to one part of an object automatically enhances perceptual processing of other parts [6*,7,8], and by demonstrating that certain effects and aftereffects of attention remain fixed to an object, even when it moves to a new location [9*,10*,11-131. Object-based attention can be thought of as a filter through which one object at a time is selected for processing by neural systems that analyze and represent object structure. The idea that the brain contains neurons with objectcentered spatial selectivity is supported by psychological experiments showing that various aftereffects are specific to the object-centered location at which a stimulus has been presented. Inhibition of return attaches to one locus on the surface of an object, traveling with that locus as the object rotates [ 14’*]. Likewise, priming effects, which build up across trials, exhibit specificity for a particular relative location within an array, even when absolute location of the array varies from trial to trial [15*,16]. Object-centered aftereffects presumably result from shifts in the tonic excitability of neurons selective for specific object-centered locations. Neurons representing different object-centered locations may be arranged in the form a map of object-centered space. Support for the existence of at least a crude map of object-centered space has arisen from an experiment suggesting that each hemisphere processes information from the contralateral half of an object or array [17*]. This conclusion is concordant with a large body of neuropsychological data reviewed in the next section.
Neuropsychology: characterizing object-centered and axis-based neglect After unilateral cortical injury, especially to the right parietal lobe, many patients manifest hemineglect, a
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Cognitive neuroscience
Figure 1 Drawings made by a patient with left object-centered neglect following right hemisphere injury. (a) In the patient’s copy, both flowers shown in the model were reproduced, but details on the left half of each flower were omitted. (b) When the same flowers were united into one plant, details on the left side of the whole plant were omitted. Adapted from Figures 1 and 3 of [18].
profound unawareness of the contralesional half of space. Recent studies have indicated that hemineglect in some patients is spatially organized with respect to the current object of regard rather than with respect to the visual field. In these patients, the line dividing the good field from the bad field runs through the center of the current object of regard (object-centered neglect) and affects the half of the object that is to the left of its intrinsic midline, even when it is tilted so that the midline is not vertical (axis-based neglect). Object-centered
neglect
Patients with left object-centered neglect (generally resulting from right hemisphere injury) may detect and copy every object in a scene, and yet, they omit details on the left half of each object, as shown in Figure 1 [18]. In copying a complex figure, they tend to omit the left half of each element in the figure, as if attention were focused on each element in succession [19]. In viewing a display that can be parsed into ‘figure’ and ‘ground’ in more than one way, these patients neglect the left half of whichever segment they have been instructed to see as the ‘figure’ [ZO,Zl~*,ZZ]. This pattern of results might
arise if patients with a simple left-hemifield impairment consistently fixated the centers of objects, thus bringing the left half of each object into the bad hemifield [23]. However, this interpretation can be ruled out by the finding that object-left impairments occur even when fixation is controlled and the whole stimulus array is confined to one hemifield [24]. Neglect for the object on which attention currently is focused can be dissociated from neglect for the surrounding field of unattended objects. This has been established in studies of two patients who neglect the left sides of objects and the right sides of surrounds [25,26]. When presented with a written word and required to read it (treating it as a unitary object), they neglect its left half. When presented with the same word and required to spell it out (treating each letter as a separate object), they neglect letters on the right. This pattern of performance is consistent with the interpretation that damage has occurred to the left half of an object map (representing the thing on which attention is focused) and to the right half of a surround map (representing unattended objects). Patients with damage to the right half
Brain representation
of a surround map, when attempting to spell out a word one letter at a time, would tend not to see, and thus not to shift attention to, letters to the right of the currently attended locus. Surround neglect has been observed in the left as well as in the right hemifield [27]. Object-centered neglect has also been revealed by tests in which patients are required to move their fingers or to sense when their hand is touched. The relative positions of a pair of points on the hand can be reversed by simply rotating the hand from a palm-up to a palm-down orientation. For example, when the right hand is pointing forward, its index finger and middle finger are located to the left and right, respectively, when the palm is down, but to the right and left, respectively, when the palm is up. Regardless of whether the palm is up or down, patients with left hemispatial neglect show deficits in performance affecting the side of the hand that is to the left. They are less likely to detect touch on the side of the wrist currently to the left [ZS*], and they are slower to initiate movements with the finger currently to the left [29@]. These findings indicate that object-centered neglect arises from a defect in the representation of object-centered space that transcends any specific sensory or motor modality. Object-centered neglect is open to at least two interpretations. The first interpretation, based on the object map model, is that damage to the right hemisphere has destroyed the left half of a map of object space. An alternative interpretation, not requiring the existence of an object map, is that damage to the right hemisphere has created an interhemispheric imbalance, giving rise to a continuous gradient of dysfunction in which the ability of stimuli to capture and hold attention decreases steadily from right to left across the visual field [30]. The second interpretation is compatible with network modeling studies showing that if images on the retina compete for attention, and if retinal loci progressively farther to the left are progressively weaker, then, when an array is presented anywhere in the visual field, the leftmost elements will fail to capture attention [31]. The phenomenon described next, axis-based neglect, is not easily accounted for in terms of a gradient of dysfunction.
Axis-based
neglect
Neglect for elements on the left side of an object might reflect an inability to see things to the left of either of two axes: first, the object’s intrinsic vertical axis, or second, the line, having a vertical orientation as defined with respect to the retina and gravity, which passes through the center of the object. These possibilities can be distinguished by rotating an object in the image plane so that the line dividing its right side from its left side is no longer vertical, as defined with respect to the retina and gravity. Studies utilizing this procedure have demonstrated that neglect, in some cases, is defined with respect to the
of object-centered
space Olson and Gettner
object’s intrinsic axis. This phenomenon ‘axis-based neglect.’
167
has been termed
In one recent study, patients with left hemineglect were induced by contextual factors to see an identical horizontal line segment as either the right or left side of a tilted equilateral triangle [32**]. Required to detect a gap in the line segment, they experienced more failures when it was seen as the left side of a triangle than when it was seen as the right side. In another experiment, patients with right parietal injury were required to detect stimuli flashed on either end of a barbell-like frame consisting of two circles connected by a horizontal line segment [33”]. On some trials, the barbell came on and then remained in place until presentation of the stimulus. On these trials, the slowest reactions were to stimuli presented in the left circle. On other trials, the barbell came on and then was rotated 180” before presentation of the stimulus. On these trials, the slowest reactions were to stimuli presented in the circle currently on the right end of the barbell. This circle, although on the right at the time of stimulus presentation, was on the left when the barbell first appeared. This result is compatible with the interpretation that neglect was defined with respect to a frame that remained fixed to the barbell as it rotated. Omitting the line connecting the circles eliminates this effect, presumably because it prevents perceiving the barbell as a unitary object [34]. Axis-based neglect, unlike object-centered neglect, cannot easily be accounted for by supposing that attention becomes progressively more impaired from one side of the visual field to the other. A gradient of dysfunction defined with respect to the retina would not rotate with the object. Demonstrations of axis-based neglect thus provide important support for the object map model.
Neurophysiology: identifying neurons with object-centered direction selectivity Several recent studies have demonstrated the existence in the brain of neurons that are object selective. In humans, a restricted area of lateroposterior occipital cortex exhibits enhanced blood flow during viewing of objects, whether represented by pictures or line drawings, but not during viewing of textures [35,36]. In the pre-motor and parietal cortex of monkeys, neurons exhibit selectivity for the three-dimensional structure of objects, firing when an object of the preferred shape is seen or grasped [37]. In the inferotemporal cortex of monkeys, neurons subserving visual pattern recognition exhibit selectivity for two-dimensional image-plane patterns [38]. The existence of object-selective neurons is of interest but does not, in itself, cast light on the validity of the object map hypothesis. The object map model requires that neurons exhibit selectivity for particular object-centered locations as opposed to particular objects. Object-centered spatial selectivity of the sort required by the model might appear in
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neuroscience
Flgure 2
(a)
500 ms
EM
EM
E-M
50 spikes s-l
4 deg EM Data from a SEF neuron selective for the object-centered direction of eye movements. (a) Each histogram represents the average firing rate, as a function of time, during trials conforming to a particular condition represented in the panel above the histogram. At the beginning of each trial, while the monkey maintained fixation on a central spot, a white target spot came on. The spot might appear in isolation (conditions A-C) or in superimposition on a horizontal bar’s right end (condition D) or left end (condition E). After a delay of around 1.5 s, the central fixation spot was extinguished and the monkey was required to make an eye movement directly to the white spot. Data from successive trials are aligned on the time of occurrence of the eye movement (EM). This neuron fired during the delay period at a rate determined by the direction of the impending eye movement. It was sensitive to the absolute direction of the eye movement, firing progressively more strongly before eye movements directed progressively farther to the right when the targets were simple spots (conditions A-C). It was also sensitive to object-centered direction, firing more strongly before an eye movement to the right end of a target bar (condition D) than before an identical eye movement to the left end of a target bar (condition E). (b) Each group of dots (A-E) represents eye position during 16 eye movements performed under the corresponding condition. Eye movements 6, D and E were nearly identical. Thus, differential activity across conditions B, D and E cannot be accounted for in terms of differences among the eye movements. Reproduced, with permission, from Figure 3 of [40”1.
sensory or motor neurons. A visual neuron, once attention has focused on an object, might respond only to something flashed at a certain location on that object, thus manifesting an object-centered visual receptive field. A motor neuron, once attention has focused on an object, might fire in conjunction only with movements directed to a certain location on that object, thus manifesting an objectcentered motor action field.
The first hint that cortical neurons might encode relative locations, if not object-centered ones, was obtained more than two decades ago. In the prefrontal cortex of monkeys trained to reach in alternation for the rightmost or leftmost of two targets, some neurons were found to fire preferentially following target-left and target-right trials, regardless of where the targets were placed relative to the monkey’s body [39]. Only recently has research
Brain representation
on neuronal encoding of object-centered locations progressed beyond this point. In area V4, neuronal visual responsiveness has been shown to depend on where the visual stimulus is located relative to the monkey’s current focus of attention, an effect which may reflect the participation of V4 neurons in encoding object-centered locations (CE Connor, DC Preddie, JL Gallant, DC Van Essen, Sot Neurosci Abstr 1995, 21:1759). Even stronger evidence for object-centered spatial selectivity has been obtained in a study of the supplementary eye field (SEF). We discovered that SEF neurons are selective for object-centered direction by monitoring their activity while monkeys made eye movements to the right or left end of a horizontal target bar [40”]. At the beginning of each two-second trial, the monkey fixated a spot at the center of the screen; then a horizontal sample bar appeared at a lateral location and a cue spot flashed on either its right or left end; a delay period ensued, during which the monkey had to remember the instruction conveyed by the sample-cue display; finally, a target bar appeared at an unpredictable location, and the monkey was required to make an eye movement to the end of the target bar matching the cued end of the sample bar. On interleaved trials, the target bar was presented at several different unpredictable locations chosen to ensure that there was no correlation across trials between the end of the bar to which the eye movement was directed (right or left end) and the physical direction of the eye movement (rightward or leftward in the orbit). The activity of most neurons studied during performance of this task depended on the end of the bar targeted by the impending eye movement. Further studies showed that object-centered direction selectivity occurs automatically. When the monkey made visually guided eye movements to salient spots superimposed on the ends of bars, a task that did not require noticing the bars or using object-centered information, neurons continued to exhibit object-centered direction selectivity (Figure 2). In each hemisphere, a majority of neurons fired most strongly before eye movements to the opposite end of the bar, in harmony with the observation that patients commonly neglect the side of an object opposite their injured hemisphere. These results provide significant support for both properties of the object map model as described in the introduction by demonstrating, first, that the brain contains neurons with object-centered direction selectivity and second, that neurons representing different object-centered directions are regionally segregated. We strongly suspect that object-centered direction selectivity is not unique to the SEF and is not restricted to neurons firing during eye movements. Our provisional interpretation is that the SEF serves as an interface between cognitive areas, which carry out an analysis of the visual scene framed in terms of object-centered space, and oculomotor centers, which generate motor commands. A
of object-centered
clear direction object-centered
space Olson and Gettner
169
for future experiments will be to search for spatial selectivity in other cortical areas.
Conclusions Recent studies have produced considerable progress in our understanding of how the brain represents objects. Studies of human performance have revealed that attention tends to focus selectively on elements that belong to a single object. Once attention has been focused on the object, its structure is represented centrally by a process that may involve projecting its normalized image onto a neural map of object-centered space. The existence of an object map is suggested by psychological and neuropsychological studies showing that each hemisphere contributes preferentially to the representation of elements in the contralateral half of the attentional window. Electrophysiological studies in monkeys have provided further support for this notion by demonstrating the existence of neurons with object-centered spatial selectivity. Future progress in this area will depend on interaction between human studies, which permit a refined analysis of spatial performance, and electrophysiological studies in animals, which permit characterizing neural mechanisms directly and unambiguously.
Acknowledgements We acknowledge support for CR Olson from the National Science Foundation (IBN 9312763) and the National Instkutes of Health CR01 NSZ7287). and for SN Gertner from the National Institutes of Health (1 F32 NSO9452) and the McDonnell-Pew Program for Cognitive Neuroscience (Individual Grant in Aid). We thank C Colby and S Kosslyn for helpful comments on the manuscript.
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Brain representation of object-centered space Carl R Olson1 and Sonya N Gettner* Object-centered spatial awareness underlies many important cognitive functions, including reading, which requires registering the locations of letters relative to a word, and pattern recognition, which requires registering the locations of features relative to a whole pattern. Recent studies have elucidated the nature of the brain mechanisms underlying this form of spatial awareness by showing that attention tends to focus on objects rather than on regions of space: by demonstrating that each hemisphere contributes selectively to awareness of the opposite half of object space, and by revealing that neurons in some cortical areas are selective for particular locations in object space. These results are concordant with the general idea that imagining or attending to an object is accompanied by projecting its image onto a neural map of object-centered space. An important aim for future studies will be to test and extend this ‘object map’ hypothesis.
Address Department of Oral and Craniofacial Biological Sciences, Room 5A12, University of Maryland Dental School, 666 West Baltimore Street, Baltimore, Maryland 21201, USA ‘e-mail: colsonQumabnet.ab.umd.edu 2e-mail: [email protected] Abbreviation supplementary eye field SEF
Current Opinion in Neurobiology
1996, 6:165-l
70
0 Current Biology Ltd ISSN 0959-4388
Introduction When we look at or think about an object, we are aware of its structure. We know, for example, that the letter ‘b’ would have to be rotated out of the page in order to transform it into the letter ‘p’. Recent work has indicated that this structural awareness may depend on a neural system with two distinctive traits: first, it contains neurons that are selective for locations as defined relative to a reference frame centered on the object itself, and second, these neurons are arranged so that their spatial fields form a map of object-centered space. The object map can be thought of as a ‘screen’ or ‘visuospatial scratchpad’ on which the image of an object is projected by scaling, translating and rotating it to produce a normalized representation [ 1,2]. The object map hypothesis is consistent with a variety of data from recent experiments in several fields. In this review, we will present findings from psychological studies indicating that attention naturally focuses on objects and on particular locations within objects.
We will then describe studies of brain-injured patients demonstrating that neglect can attach to one half of an object rather than to one half of the body or of external recording space. Finally, we will discuss single-neuron studies showing that neurons in some cortical areas are selective for spatial locations as defined with respect to an object-centered reference frame.
Psychology: showing that attention to objects
attaches
The first step toward forming a mental representation of an object is to attend to it. Attention is specifically object based, rather than space based, in the sense that at any given moment it tends to focus on elements that belong to one object, excluding even overlapping or interspersed elements that are not part of that object [3-S]. Recent experiments have strengthened the view that attention is object based by showing that attention to one part of an object automatically enhances perceptual processing of other parts [6*,7,8], and by demonstrating that certain effects and aftereffects of attention remain fixed to an object, even when it moves to a new location [9*,10*,11-131. Object-based attention can be thought of as a filter through which one object at a time is selected for processing by neural systems that analyze and represent object structure. The idea that the brain contains neurons with objectcentered spatial selectivity is supported by psychological experiments showing that various aftereffects are specific to the object-centered location at which a stimulus has been presented. Inhibition of return attaches to one locus on the surface of an object, traveling with that locus as the object rotates [ 14’*]. Likewise, priming effects, which build up across trials, exhibit specificity for a particular relative location within an array, even when absolute location of the array varies from trial to trial [15*,16]. Object-centered aftereffects presumably result from shifts in the tonic excitability of neurons selective for specific object-centered locations. Neurons representing different object-centered locations may be arranged in the form a map of object-centered space. Support for the existence of at least a crude map of object-centered space has arisen from an experiment suggesting that each hemisphere processes information from the contralateral half of an object or array [17*]. This conclusion is concordant with a large body of neuropsychological data reviewed in the next section.
Neuropsychology: characterizing object-centered and axis-based neglect After unilateral cortical injury, especially to the right parietal lobe, many patients manifest hemineglect, a
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Cognitive neuroscience
Figure 1 Drawings made by a patient with left object-centered neglect following right hemisphere injury. (a) In the patient’s copy, both flowers shown in the model were reproduced, but details on the left half of each flower were omitted. (b) When the same flowers were united into one plant, details on the left side of the whole plant were omitted. Adapted from Figures 1 and 3 of [18].
profound unawareness of the contralesional half of space. Recent studies have indicated that hemineglect in some patients is spatially organized with respect to the current object of regard rather than with respect to the visual field. In these patients, the line dividing the good field from the bad field runs through the center of the current object of regard (object-centered neglect) and affects the half of the object that is to the left of its intrinsic midline, even when it is tilted so that the midline is not vertical (axis-based neglect). Object-centered
neglect
Patients with left object-centered neglect (generally resulting from right hemisphere injury) may detect and copy every object in a scene, and yet, they omit details on the left half of each object, as shown in Figure 1 [18]. In copying a complex figure, they tend to omit the left half of each element in the figure, as if attention were focused on each element in succession [19]. In viewing a display that can be parsed into ‘figure’ and ‘ground’ in more than one way, these patients neglect the left half of whichever segment they have been instructed to see as the ‘figure’ [ZO,Zl~*,ZZ]. This pattern of results might
arise if patients with a simple left-hemifield impairment consistently fixated the centers of objects, thus bringing the left half of each object into the bad hemifield [23]. However, this interpretation can be ruled out by the finding that object-left impairments occur even when fixation is controlled and the whole stimulus array is confined to one hemifield [24]. Neglect for the object on which attention currently is focused can be dissociated from neglect for the surrounding field of unattended objects. This has been established in studies of two patients who neglect the left sides of objects and the right sides of surrounds [25,26]. When presented with a written word and required to read it (treating it as a unitary object), they neglect its left half. When presented with the same word and required to spell it out (treating each letter as a separate object), they neglect letters on the right. This pattern of performance is consistent with the interpretation that damage has occurred to the left half of an object map (representing the thing on which attention is focused) and to the right half of a surround map (representing unattended objects). Patients with damage to the right half
Brain representation
of a surround map, when attempting to spell out a word one letter at a time, would tend not to see, and thus not to shift attention to, letters to the right of the currently attended locus. Surround neglect has been observed in the left as well as in the right hemifield [27]. Object-centered neglect has also been revealed by tests in which patients are required to move their fingers or to sense when their hand is touched. The relative positions of a pair of points on the hand can be reversed by simply rotating the hand from a palm-up to a palm-down orientation. For example, when the right hand is pointing forward, its index finger and middle finger are located to the left and right, respectively, when the palm is down, but to the right and left, respectively, when the palm is up. Regardless of whether the palm is up or down, patients with left hemispatial neglect show deficits in performance affecting the side of the hand that is to the left. They are less likely to detect touch on the side of the wrist currently to the left [ZS*], and they are slower to initiate movements with the finger currently to the left [29@]. These findings indicate that object-centered neglect arises from a defect in the representation of object-centered space that transcends any specific sensory or motor modality. Object-centered neglect is open to at least two interpretations. The first interpretation, based on the object map model, is that damage to the right hemisphere has destroyed the left half of a map of object space. An alternative interpretation, not requiring the existence of an object map, is that damage to the right hemisphere has created an interhemispheric imbalance, giving rise to a continuous gradient of dysfunction in which the ability of stimuli to capture and hold attention decreases steadily from right to left across the visual field [30]. The second interpretation is compatible with network modeling studies showing that if images on the retina compete for attention, and if retinal loci progressively farther to the left are progressively weaker, then, when an array is presented anywhere in the visual field, the leftmost elements will fail to capture attention [31]. The phenomenon described next, axis-based neglect, is not easily accounted for in terms of a gradient of dysfunction.
Axis-based
neglect
Neglect for elements on the left side of an object might reflect an inability to see things to the left of either of two axes: first, the object’s intrinsic vertical axis, or second, the line, having a vertical orientation as defined with respect to the retina and gravity, which passes through the center of the object. These possibilities can be distinguished by rotating an object in the image plane so that the line dividing its right side from its left side is no longer vertical, as defined with respect to the retina and gravity. Studies utilizing this procedure have demonstrated that neglect, in some cases, is defined with respect to the
of object-centered
space Olson and Gettner
object’s intrinsic axis. This phenomenon ‘axis-based neglect.’
167
has been termed
In one recent study, patients with left hemineglect were induced by contextual factors to see an identical horizontal line segment as either the right or left side of a tilted equilateral triangle [32**]. Required to detect a gap in the line segment, they experienced more failures when it was seen as the left side of a triangle than when it was seen as the right side. In another experiment, patients with right parietal injury were required to detect stimuli flashed on either end of a barbell-like frame consisting of two circles connected by a horizontal line segment [33”]. On some trials, the barbell came on and then remained in place until presentation of the stimulus. On these trials, the slowest reactions were to stimuli presented in the left circle. On other trials, the barbell came on and then was rotated 180” before presentation of the stimulus. On these trials, the slowest reactions were to stimuli presented in the circle currently on the right end of the barbell. This circle, although on the right at the time of stimulus presentation, was on the left when the barbell first appeared. This result is compatible with the interpretation that neglect was defined with respect to a frame that remained fixed to the barbell as it rotated. Omitting the line connecting the circles eliminates this effect, presumably because it prevents perceiving the barbell as a unitary object [34]. Axis-based neglect, unlike object-centered neglect, cannot easily be accounted for by supposing that attention becomes progressively more impaired from one side of the visual field to the other. A gradient of dysfunction defined with respect to the retina would not rotate with the object. Demonstrations of axis-based neglect thus provide important support for the object map model.
Neurophysiology: identifying neurons with object-centered direction selectivity Several recent studies have demonstrated the existence in the brain of neurons that are object selective. In humans, a restricted area of lateroposterior occipital cortex exhibits enhanced blood flow during viewing of objects, whether represented by pictures or line drawings, but not during viewing of textures [35,36]. In the pre-motor and parietal cortex of monkeys, neurons exhibit selectivity for the three-dimensional structure of objects, firing when an object of the preferred shape is seen or grasped [37]. In the inferotemporal cortex of monkeys, neurons subserving visual pattern recognition exhibit selectivity for two-dimensional image-plane patterns [38]. The existence of object-selective neurons is of interest but does not, in itself, cast light on the validity of the object map hypothesis. The object map model requires that neurons exhibit selectivity for particular object-centered locations as opposed to particular objects. Object-centered spatial selectivity of the sort required by the model might appear in
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Cognitive
neuroscience
Flgure 2
(a)
500 ms
EM
EM
E-M
50 spikes s-l
4 deg EM Data from a SEF neuron selective for the object-centered direction of eye movements. (a) Each histogram represents the average firing rate, as a function of time, during trials conforming to a particular condition represented in the panel above the histogram. At the beginning of each trial, while the monkey maintained fixation on a central spot, a white target spot came on. The spot might appear in isolation (conditions A-C) or in superimposition on a horizontal bar’s right end (condition D) or left end (condition E). After a delay of around 1.5 s, the central fixation spot was extinguished and the monkey was required to make an eye movement directly to the white spot. Data from successive trials are aligned on the time of occurrence of the eye movement (EM). This neuron fired during the delay period at a rate determined by the direction of the impending eye movement. It was sensitive to the absolute direction of the eye movement, firing progressively more strongly before eye movements directed progressively farther to the right when the targets were simple spots (conditions A-C). It was also sensitive to object-centered direction, firing more strongly before an eye movement to the right end of a target bar (condition D) than before an identical eye movement to the left end of a target bar (condition E). (b) Each group of dots (A-E) represents eye position during 16 eye movements performed under the corresponding condition. Eye movements 6, D and E were nearly identical. Thus, differential activity across conditions B, D and E cannot be accounted for in terms of differences among the eye movements. Reproduced, with permission, from Figure 3 of [40”1.
sensory or motor neurons. A visual neuron, once attention has focused on an object, might respond only to something flashed at a certain location on that object, thus manifesting an object-centered visual receptive field. A motor neuron, once attention has focused on an object, might fire in conjunction only with movements directed to a certain location on that object, thus manifesting an objectcentered motor action field.
The first hint that cortical neurons might encode relative locations, if not object-centered ones, was obtained more than two decades ago. In the prefrontal cortex of monkeys trained to reach in alternation for the rightmost or leftmost of two targets, some neurons were found to fire preferentially following target-left and target-right trials, regardless of where the targets were placed relative to the monkey’s body [39]. Only recently has research
Brain representation
on neuronal encoding of object-centered locations progressed beyond this point. In area V4, neuronal visual responsiveness has been shown to depend on where the visual stimulus is located relative to the monkey’s current focus of attention, an effect which may reflect the participation of V4 neurons in encoding object-centered locations (CE Connor, DC Preddie, JL Gallant, DC Van Essen, Sot Neurosci Abstr 1995, 21:1759). Even stronger evidence for object-centered spatial selectivity has been obtained in a study of the supplementary eye field (SEF). We discovered that SEF neurons are selective for object-centered direction by monitoring their activity while monkeys made eye movements to the right or left end of a horizontal target bar [40”]. At the beginning of each two-second trial, the monkey fixated a spot at the center of the screen; then a horizontal sample bar appeared at a lateral location and a cue spot flashed on either its right or left end; a delay period ensued, during which the monkey had to remember the instruction conveyed by the sample-cue display; finally, a target bar appeared at an unpredictable location, and the monkey was required to make an eye movement to the end of the target bar matching the cued end of the sample bar. On interleaved trials, the target bar was presented at several different unpredictable locations chosen to ensure that there was no correlation across trials between the end of the bar to which the eye movement was directed (right or left end) and the physical direction of the eye movement (rightward or leftward in the orbit). The activity of most neurons studied during performance of this task depended on the end of the bar targeted by the impending eye movement. Further studies showed that object-centered direction selectivity occurs automatically. When the monkey made visually guided eye movements to salient spots superimposed on the ends of bars, a task that did not require noticing the bars or using object-centered information, neurons continued to exhibit object-centered direction selectivity (Figure 2). In each hemisphere, a majority of neurons fired most strongly before eye movements to the opposite end of the bar, in harmony with the observation that patients commonly neglect the side of an object opposite their injured hemisphere. These results provide significant support for both properties of the object map model as described in the introduction by demonstrating, first, that the brain contains neurons with object-centered direction selectivity and second, that neurons representing different object-centered directions are regionally segregated. We strongly suspect that object-centered direction selectivity is not unique to the SEF and is not restricted to neurons firing during eye movements. Our provisional interpretation is that the SEF serves as an interface between cognitive areas, which carry out an analysis of the visual scene framed in terms of object-centered space, and oculomotor centers, which generate motor commands. A
of object-centered
clear direction object-centered
space Olson and Gettner
169
for future experiments will be to search for spatial selectivity in other cortical areas.
Conclusions Recent studies have produced considerable progress in our understanding of how the brain represents objects. Studies of human performance have revealed that attention tends to focus selectively on elements that belong to a single object. Once attention has been focused on the object, its structure is represented centrally by a process that may involve projecting its normalized image onto a neural map of object-centered space. The existence of an object map is suggested by psychological and neuropsychological studies showing that each hemisphere contributes preferentially to the representation of elements in the contralateral half of the attentional window. Electrophysiological studies in monkeys have provided further support for this notion by demonstrating the existence of neurons with object-centered spatial selectivity. Future progress in this area will depend on interaction between human studies, which permit a refined analysis of spatial performance, and electrophysiological studies in animals, which permit characterizing neural mechanisms directly and unambiguously.
Acknowledgements We acknowledge support for CR Olson from the National Science Foundation (IBN 9312763) and the National Instkutes of Health CR01 NSZ7287). and for SN Gertner from the National Institutes of Health (1 F32 NSO9452) and the McDonnell-Pew Program for Cognitive Neuroscience (Individual Grant in Aid). We thank C Colby and S Kosslyn for helpful comments on the manuscript.
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