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Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex.

ABSTRACT: Posterior parietal cortex has been traditionally associated with perceptual attention and sensory-motor processing, but recent studies also indicate a potential role in episodic memory retrieval. Here, we developed a new paradigm to isolate top-down attention-related activity directed to either memory or perceptual information. We demonstrated a robust topographic separation in human posterior parietal cortex associated with searching for task-relevant information in episodic memory or in the environment. Control analyses confirmed that this difference was not dependent on differences in sensory stimulation or eye movements across tasks. Notably, we observed in memory- and perception-related regions a mechanism of reciprocal dynamic competition that was related to behavioral performance. These results provide the first evidence for a double dissociation between parietal networks involved in top-down attention to memory and the environment and support the idea of neural competition between perception and memory.

SUBMITTER: Sestieri C

PROVIDER: S-EPMC2906749 | biostudies-literature | 2010 Jun

REPOSITORIES: biostudies-literature

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Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex.

Sestieri Carlo C Shulman Gordon L GL Corbetta Maurizio M

The Journal of neuroscience : the official journal of the Society for Neuroscience 20100601 25

Posterior parietal cortex has been traditionally associated with perceptual attention and sensory-motor processing, but recent studies also indicate a potential role in episodic memory retrieval. Here, we developed a new paradigm to isolate top-down attention-related activity directed to either memory or perceptual information. We demonstrated a robust topographic separation in human posterior parietal cortex associated with searching for task-relevant information in episodic memory or in the en ...[more]

PMID: 20573892

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Project description:Recent models of human posterior parietal cortex (PPC) have variously emphasized its role in spatial perception, visuomotor control or directing attention. However, neuroimaging and lesion studies also suggest that the right PPC might play a special role in maintaining an alert state. Previously, assessments of right-hemisphere patients with hemispatial neglect have revealed significant overall deficits on vigilance tasks, but to date there has been no demonstration of a deterioration of performance over time--a vigilance decrement--considered by some to be a key index of a deficit in maintaining attention. Moreover, sustained attention deficits in neglect have not specifically been related to PPC lesions, and it remains unclear whether they interact with spatial impairments in this syndrome. Here we examined the ability of right-hemisphere patients with neglect to maintain attention, comparing them to stroke controls and healthy individuals. We found evidence of an overall deficit in sustaining attention associated with PPC lesions, even for a simple detection task with stimuli presented centrally. In a second experiment, we demonstrated a vigilance decrement in neglect patients specifically only when they were required to maintain attention to spatial locations, but not verbal material. Lesioned voxels in the right PPC spanning a region between the intraparietal sulcus and inferior parietal lobe were significantly associated with this deficit. Finally, we compared performance on a task that required attention to be maintained either to visual patterns or spatial locations, matched for task difficulty. Again, we found a vigilance decrement but only when attention had to be maintained on spatial information. We conclude that sustaining attention to spatial locations is a critical function of the human right PPC which needs to be incorporated into models of normal parietal function as well as those of the clinical syndrome of hemispatial neglect.

Project description:The visual system uses two complimentary strategies to process multiple objects simultaneously within a scene and update their spatial positions in real time. It either uses selective attention to individuate a complex, dynamic scene into a few focal objects (i.e., object individuation), or it represents multiple objects as an ensemble by distributing attention more globally across the scene (i.e., ensemble grouping). Neural oscillations may be a key signature for focal object individuation versus distributed ensemble grouping, because they are thought to regulate neural excitability over visual areas through inhibitory control mechanisms. We recorded whole-head MEG data during a multiple-object tracking paradigm, in which human participants (13 female, 11 male) switched between different instructions for object individuation and ensemble grouping on different trials. The stimuli, responses, and the demand to keep track of multiple spatial locations over time were held constant between the two conditions. We observed increased ?-band power (9-13 Hz) packed into oscillatory bursts in bilateral inferior parietal cortex during multiple-object processing. Single-trial analysis revealed greater burst occurrences on object individuation versus ensemble grouping trials. By contrast, we found no differences using standard analyses on across-trials averaged ?-band power. Moreover, the bursting effects occurred only below/at, but not above, the typical capacity limits for multiple-object processing (at ?4 objects). Our findings reveal the real-time neural correlates underlying the dynamic processing of multiple-object scenarios, which are modulated by grouping strategies and capacity. They support a rhythmic, ?-pulsed organization of dynamic attention to multiple objects and ensembles.SIGNIFICANCE STATEMENT Dynamic multiple-object scenarios are an important problem in real-world and computer vision. They require keeping track of multiple objects as they move through space and time. Such problems can be solved in two ways: One can individuate a scene object by object, or alternatively group objects into ensembles. We observed greater occurrences of ?-oscillatory burst events in parietal cortex for processing objects versus ensembles and below/at versus above processing capacity. These results demonstrate a unique top-down mechanism by which the brain dynamically adjusts its computational level between objects and ensembles. They help to explain how the brain copes with its capacity limitations in real-time environments and may lead the way to technological innovations for time-critical video analysis in computer vision.

Dataset Information

Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex.

Publications

Attention to memory and the environment: functional specialization and dynamic competition in human posterior parietal cortex.

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