Intact haptic priming in normal aging and Alzheimer’s disease: evidence for dissociable memory systems

Abstract

This study is the first to report complete priming in Alzheimer’s disease (AD) patients and older control subjects for objects presented haptically. To investigate possible dissociations between implicit and explicit objects representations, young adults, Alzheimer’s patients, and older controls performed a speeded object naming task followed by a recognition task. Similar haptic priming was exhibited by the three groups, although young adults responded faster than the two older groups. Furthermore, there was no difference in performance between the two healthy groups. On the other hand, younger and older healthy adults did not differ on explicit recognition while, as expected, AD patients were highly impaired. The double dissociation suggests that different memory systems mediate both types of memory tasks. The preservation of intact haptic priming in AD provides strong support to the idea that object implicit memory is mediated by a memory system that is different from the medial–temporal diencephalic system underlying explicit memory, which is impaired early in AD. Recent imaging and behavioral studies suggest that the implicit memory system may depend on extrastriate areas of the occipital cortex although somatosensory cortical mechanisms may also be involved.

Introduction

In this report, we present results from a study that investigated the status of implicit memory for familiar objects presented haptically in Alzheimer’s disease (AD) patients and older controls. In addition, a group of young adults participated in the study. We also looked at the dissociation between implicit and explicit haptic memory measures. As far as we know, this is the first study to assess haptic implicit memory in AD.

Human vision is a remarkable perceptual modality that allows one to acquire very fast and precise information from environmental objects and their spatial relations. Active touch (haptics) is a complex perceptual system that encodes information from cutaneous and kinesthetic receptors (Loomis & Lederman, 1986). This modality has proved to be very efficient in object identification (Klatzky, Lederman, & Metzger, 1985). Humans extract precise information on a number of properties of shape such as bilateral symmetry using just active touch (Ballesteros et al., 1997, Ballesteros et al., 1998; Ballesteros & Reales, in press).

Memory is not a unitary process. Multiple memory systems mediate different types of memories (Gabrieli, 1998, Schacter, 1987, Squire, 1992). Explicit memory, usually assessed by free recall, cued recall, and recognition tests, requires the conscious recollection of previous experience. This type of memory is highly impaired in Alzheimer’s disease patients and is usually the first symptom of dementia. In contrast, implicit memory refers to previous experience with stimuli that does not require intentional, conscious retrieval of previously encoded stimuli. This type of memory is assessed by indirect or implicit tests with no reference to previous experience. The usual way to demonstrate implicit memory is by showing repetition priming effects; that is, better performance in accuracy or response time for old stimuli (previously encoded) compared to new stimuli. Perceptual priming has long-lasting effects and relies on processing physical characteristics of the encoded stimuli (Schacter, Cooper, & Delaney, 1990). Implicit memory has been studied in both visual and auditory spheres. However, tactual memory is rarely studied implicitly or explicitly.

Age invariance usually exists in implicit memory tasks (Mitchell, 1989; Prull, Gabrieli, & Bunge, 2000; Schacter, 1987). Older and young adults show often similar levels of perceptual priming although the former may have some difficulties remembering new facts and events purposively (La Voie & Light, 1994, Light, 1991). The effects of age are generally not significant and when they exist are much smaller than in explicit memory tests. The stimuli commonly used in these aging studies were words and, less often, visual pictures.

AD, the most common type of senile dementia, is the fourth leading cause of death in older adults. Its central characteristic is a progressive disruption of most cognitive processes. Although there are a lot of individual differences in the course of this dementia, explicit memory deficits appear early in the course of the disease (Bondi & Kaszniak, 1991, Fleischman & Gabrieli, 1998; Huberman, Moscovith, & Friedman, 1994).

Contrasting with the clear picture from explicit memory tests, the results from implicit memory studies in AD are controversial. The discrepant results have been attributed to the heterogeneity of participants and the specific characteristics of the implicit tasks. The exhaustive review conducted by Fleischman and Gabrieli (1998) showed that approximately 85% of the studies conducted with healthy aging adults reported age invariance in priming. Regarding AD patients, around 65% of the studies reported intact perceptual priming on visual tasks such as word identification (Keane, Gabrieli, Growdon, & Corkin, 1994) and picture naming (Gabrieli et al., 1999). However, AD patients were impaired on word-stem completion (Russo & Spinnler, 1994) and picture completion tasks (Heindel, Salmon, & Butters, 1990). Gabrieli and his colleagues (Fleischman et al., 2001, Gabrieli et al., 1994, Gabrieli et al., 1999) proposed the identification–production distinction to explain the pattern of impaired and unimpaired priming obtained in some AD studies.

Patients with AD provide a useful model for investigating the neural bases of implicit and explicit memory for haptic objects because it is well known that these patients suffer, early in the disease, lesions in neocortical regions of the frontal, parietal, and temporal lobes. However, the posterior parts of the cortex are related to low-level, unimodal sensory areas and are relatively spared at early stages of this dementia (Arnold, Hyman, Flory, Damasio, & Van Hoesen, 1991).

In this study, we aimed to examine whether implicit memory for haptic objects is spared in AD patients compared to healthy controls. Based on the identification–production distinction (Gabrieli et al., 1999) and in the perceptual character of repetition priming, we hypothesized that AD patients and healthy older controls would show intact perceptual priming in a haptic identification task and impaired recognition. Such a dissociation between the implicit (speeded object naming) and the explicit memory (old–new recognition) tasks would indicate that the two types of memories are mediated by different memory systems in the brain.