Elsevier

Neuropsychologia

Volume 46, Issue 12, October 2008, Pages 2943-2948
Neuropsychologia

Modulation of the spatial attention network by incentives in healthy aging and mild cognitive impairment

https://doi.org/10.1016/j.neuropsychologia.2008.06.005Get rights and content

Abstract

Impairments of spatial attention are common in Alzheimer's disease (AD), but may develop earlier in the course of the disease, a condition referred to as mild cognitive impairment (MCI). In a previous experiment, we showed that emotional content overcame the AD-related decline in selective attention to novel events [LaBar, K. S., Mesulam, M., Gitelman, D. R., & Weintraub, S. (2000). Emotional curiosity: Modulation of visuospatial attention by arousal is preserved in aging and early-stage Alzheimer's disease. Neuropsychologia, 38(13), 1734–1740]. The current experiment examined the influence of secondary reinforcers upon selective spatial attention in MCI and healthy aging (EC). Subjects performed a covert attention task while undergoing fMRI. They won money for fast responses and lost money for slow responses. In young subjects, this task had shown that the influence of incentive upon spatial attention is mediated by the posterior cingulate (PCC) and orbitofrontal cortices (OFC) [Small, D. M., Gitelman, D., Simmons, K., Bloise, S. M., Parrish, T., & Mesulam, M. M. (2005). Monetary incentives enhance processing in brain regions mediating top-down control of attention. Cerebral Cortex, 15(12), 1855–1865]. Both groups were able to use spatial cues to generate an anticipatory attentional shift towards the cued location. The prospect of winning (but not losing) money enhanced attentional shifts in EC subjects, an effect that was mediated by OFC activation. In contrast, only the prospect of losing money enhanced attentional shifts in MCI subjects, an effect that correlated with PCC activation. Behavioral effects of incentive upon spatial attention are only partially maintained in EC and MCI with corresponding modifications in the underlying neural circuitry. These results suggest a reorganization of the relationships between the limbic system and spatial attention network in healthy aging and MCI.

Introduction

Attention is among the first non-memory cognitive functions to be impaired in early Alzheimer's disease (AD) and evidence exists for a variety of attentional impairments including; difficulty disengaging attention and shifting attentional focus towards new locations (Parasuraman, Greenwood, Haxby, & Grady, 1992); disrupted search architecture, as indicated by inefficient deployment of fixations within the effective work space (Rosler et al., 2000); and decreased novelty-seeking when given a choice to look at conventional versus incongruous stimuli (Daffner, Scinto, Weintraub, Guinessey, & Mesulam, 1992). This latter deficit can be overcome by increasing the motivational saliency of the attentional targets. LaBar, Mesulam, Gitelman, and Weintraub (2000) showed that AD patients paid as much preferential attention to emotionally arousing stimuli as age-matched controls.

The aim of the current study was to test whether subtle secondary reinforcers, such as monetary incentives, could also overcome attentional deficits in the prodromal stage of AD known as amnestic mild cognitive impairment (MCI). We used fMRI to explore the functional anatomy of attentional processes and their modulation by incentive in healthy aging and MCI within the context of a task and spatial attention network that has been previously investigated in young, neurologically intact subjects. The task was a modified version of the “Posner task”, which measures lateral shifts in the attentional focus (Posner, 1980). Spatial cues presented at central fixation, direct attention to a peripheral location (left or right) where a target is expected to appear after an interval of 200–800 ms. The task is to respond to the stimulus that appears in one of the peripheral locations as rapidly as possible if it is a target (an ‘X’) but not at all if it is a foil (a ‘+’). In most trials, the stimulus appears in the cued direction, in which case it is referred to as a validly cued trial. In a small number of trials, the stimulus appears in the opposite direction, requiring the subject to reorient attention to the contralateral side. These are referred to as invalidly cued trials. Reaction times (RTs) to target detection in validly cued trials are consistently found to be shorter than those to target detection in invalidly cued trials (Posner, 1980). It is assumed that the basis for the reduced RT is a cue-induced anticipatory attentional shift, with the difference between RT reflecting the effectiveness of anticipatory attention. In young subjects, the prospect of winning or the threat of losing money enhances the efficiency of anticipatory attentional shifts (Small et al., 2005). Specifically, gain- or loss-induced enhancements of attentional shifting are correlated with neural activity in PCC while gain-induced enhancements were also correlated with activity in the OFC (Small et al., 2005). There is evidence that the PCC and OFC are compromised very early in the course of the development of AD pathology. For example, the PCC is one of the earliest areas to show hypometabolism in AD (Ishii et al., 1997, Minoshima et al., 1997), and the OFC is second only to the medial temporal cortex in the density of neurofibrillary tangles it contains, even during cognitively normal aging and MCI (Guillozet, Weintraub, Mash, & Mesulam, 2003). Therefore, we were particularly interested in the potential for re-organization of the relationships between the limbic system and spatial attention network in healthy aging and MCI.

Section snippets

Participants

Twelve MCI patients and 12 age-matched controls were recruited from the Northwestern Alzheimer's Disease Center Clinical Core registry, based on their level of cognitive performance as assessed with neuropsychological testing and neurological examination. These include the Mini Mental State Examination (MMSE) (Folstein, Folstein, & McHugh, 1975), the Clinical Dementia Rating (CDR) (Morris, 1997) and several subtests from the Consortium to Establish a Registry for Alzheimer's Disease (CERAD) (

Behavioral data

The ANOVA of RT data revealed a main effect for trial type {F(2,56) 32.3, p = 5 × 10−10} and planned comparisons between valid and non-directional cues as well as invalid and non-directional cues illustrated that valid cues generated the fastest target detection time compared to non-directional cues (p < 6 × 10−4), whereas invalid cues caused the slowest target detection time compared with non-directional cues (p = 5 × 10−6). These results illustrate that both groups demonstrated decreased RT to detect

Discussion

Despite the extensive perturbations of spatial attention that are known to arise in aging and MCI (Parasuraman et al., 1992, Rosler et al., 2000), we found that these subjects are able to use a central directional cue to shift attention to a peripheral location, as shown by the presence of a validity effect and cue benefit. In the normal brain, spatial attention is controlled by a large scale network of distributed regions in parietal, frontal, and paralimbic cortices (Mesulam, 1981, Mesulam,

Acknowledgements

This study was conducted at Northwestern University's Feinberg School of Medicine Cognitive Neurology and Alzheimer's Disease Center.

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