Research report
Facial expression decoding in early Parkinson's disease

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Abstract

The ability to derive emotional and non-emotional information from unfamiliar, static faces was evaluated in 21 adults with idiopathic Parkinson's disease (PD) and 21 healthy control subjects. Participants' sensitivity to emotional expressions was comprehensively assessed in tasks of discrimination, identification, and rating of five basic emotions: happiness, (pleasant) surprise, anger, disgust, and sadness. Subjects also discriminated and identified faces according to underlying phonemic (“facial speech”) cues and completed a neuropsychological test battery. Results uncovered limited evidence that the processing of emotional faces differed between the two groups in our various conditions, adding to recent arguments that these skills are frequently intact in non-demented adults with PD [R. Adolphs, R. Schul, D. Tranel, Intact recognition of facial emotion in Parkinson's disease, Neuropsychology 12 (1998) 253–258]. Patients could also accurately interpret facial speech cues and discriminate the identity of unfamiliar faces in a normal manner. There were some indications that basal ganglia pathology in PD contributed to selective difficulties recognizing facial expressions of disgust, consistent with a growing literature on this topic. Collectively, findings argue that abnormalities for face processing are not a consistent or generalized feature of medicated adults with mild-moderate PD, prompting discussion of issues that may be contributing to heterogeneity within this literature. Our results imply a more limited role for the basal ganglia in the processing of emotion from static faces relative to speech prosody, for which the same PD patients exhibited pronounced deficits in a parallel set of tasks [M.D. Pell, C. Leonard, Processing emotional tone from speech in Parkinson's disease: a role for the basal ganglia, Cogn. Affect. Behav. Neurosci. 3 (2003) 275–288]. These diverging patterns allow for the possibility that basal ganglia mechanisms are more engaged by temporally-encoded social information derived from cue sequences over time.

Introduction

Abnormalities in face processing have been cited as one of the cognitive sequelae of idiopathic Parkinson's disease (PD) without dementia [26], [28], [45]. Human faces are subject to an array of processes that are thought to be modular in structure [18], [19] and which fractionate in various ways in the context of acquired brain illnesses such as PD [23], [25], [40], [65]. According to Bruce and Young's well-known model [18], functional components of the face processing system include the ability to detect familiarity about known faces based on their structural properties and to make various ‘semantic’ judgements about the sex, age, intelligence, and trustworthiness of individuals whose face is encountered, to name but a few. Of key interest here, the early structural elaboration of faces serves as the foundation for deriving two distinct ‘codes’ that are largely independent of recognizing the identity or familiarity of a face: a code for deriving the emotional expression or meaning of the face; and facial speech codes that facilitate linguistic processes of speech perception during verbal discourse [18], [23]. These latter two functional components permit key inferences to be drawn about faces that shape communicative interactions and interpersonal behavior; given the paramount social importance of these functions, coupled with claims that face processing is frequently affected by PD, the present study sought to investigate these functions in the context of PD in a more comprehensive manner.

While the integrity of face processing skills in PD has been called into question, relevant findings are still limited and conclusions about what processes are affected are decidedly mixed. An influential study conducted by Dewick, Hanley, Davies and colleagues [28] tested a range of face processing skills in non-demented adults with and without PD, involving: discrimination, matching, and short-term recall of unfamiliar faces by their identity; discrimination of faces by sex or emotion expression; and discrimination of visually-articulated speech sounds (i.e., facial speech processing or “speech-reading”). With the exception of the emotion task which yielded a ceiling effect for both groups, individuals with PD were significantly impaired in all conditions, a finding the authors attributed to a basic deficit in the structural encoding of faces. The investigators argued that processing of emotion expressions would have been negatively affected by such a deficit but that their emotion task was insensitive to these processes in the PD group. The idea that PD is associated with relatively basic defects in the visual perceptual (i.e., structural) analysis of faces, with repercussions at later stages of encoding for these events, echoes earlier results for 43 PD patients studied by Beatty et al. [10] and is supported by some recent work [26], [34]. When this hypothesis has been examined in greater detail [26], there are indications that structural processing failures in PD may center around visual tasks of configural rather than componential processing of faces, especially when facial stimuli are degraded in some way (e.g., black and white line drawings).

Not all findings indicate that face processing difficulties in PD are manifested at the level of structural encoding. For instance, Jacobs et al. [41] noted that 12 PD patients could accurately discriminate unfamiliar faces by their distinguishing properties (identity) but not by emotional expression. Sprengelmeyer and colleagues [60] also described groups of medicated and unmedicated adults with PD who could normally discriminate unfamiliar faces by identity or sex, but who displayed specific impairments in the recognition of emotional faces taken from the Ekman and Friesen [30] series. Results of these and other studies [16], [42] are more conducive to a specific emotional face processing deficit in PD. In the Sprengelmeyer et al. investigation, which is the sole one to date to examine face processing abilities in unmedicated as well as medicated PD patients, the influence of dopamine status on emotional face processing in PD was strongly highlighted; L-dopa therapy appeared to diminish the severity of deficits for recognizing particular expressions of emotion such as disgust in medicated patients, in spite of the advanced stage of disease in this group. The possibility that recognizing specific emotional expressions such as disgust is critically reliant on the intact basal ganglia, and therefore susceptible to disruption in PD and other disorders of these structures, is a claim that has been proposed on several occasions [20], [31], [33], [59], [63] and should be monitored further.

Still other, well-controlled studies have identified little evidence that emotional face processing is disturbed in a detectable manner by PD. For example, there are two reports that the ability to label the six basic emotions from the Ekman series is intact in mild-moderate PD without dementia [14], [61]. Borod et al. further noted that the discrimination of serially-presented emotional face expressions was intact in her sample of 20 adults with PD, consistent with Dewick et al.'s earlier observations. Adolphs et al. [6] required 18 PD patients to complete the Benton face discrimination task and an emotional rating paradigm in which subjects judged the presence of pre-designated emotional attributes of Ekman faces along an intensity continuum (this paradigm provides a more sensitive index of emotional processes in PD according to the researchers). This investigation revealed no indications that PD patients were deficient in either the structural or emotional face processing task, questioning the actual extent to which basal ganglia degeneration and associated pathology in PD are tied to deficits in (emotional) face processing. The possibility that PD yields a more selective pattern of emotion deficits, affecting knowledge about only specific emotions such as disgust, was also not strongly indicated by their data [6] or by some other PD studies that have tested the recognition of disgust [10], [14], [29].

Equivocal claims about the status and specificity of emotional face processing deficits in PD call for additional, fine-grained evaluation of these skills in a well-defined patient sample. The goals of this study were to establish how individuals in the early stages of PD interpret the emotional value of faces in different task processing contexts that require them to discriminate, identify/label, or rate emotional features along an intensity gradient; concurrently, we examined how well these patients process non-emotional facial information (facial speech cues) that can also be derived from the structural description of faces [18]. Data from both experimental conditions were interpreted in light of a selected battery of neuropsychological background tests, including the ability to discriminate structural descriptions of faces by their physical identity. Our testing incorporated a series of perceptually-validated, color face stimuli [53] to extend previous findings on PD to a new set of items and to establish a tight comparison between abilities on emotional face expression, facial speech processing, and emotional prosody [55] tasks which employed stimuli posed by the same actors.

Despite the undisputedly mixed findings to date, we hypothesized that PD status would be associated with deficits on certain emotional processing tasks, particularly the identification of facial expressions of emotion from an array of verbal response alternatives [16], [42], [60]. In the absence of detailed information on how PD patients decode facial speech information as an independent function, we predicted that deficits in the processing of both emotional and non-emotional faces, if observed, would bear a strong relationship to underlying cognitive features of our PD participants, especially the ability to structurally encode faces (as indexed through background measures such as the Benton face discrimination subtest). The possibility that basal ganglia damage in PD might selectively influence the perception of disgust or anger faces was also considered relevant in face of a growing literature on this topic. Finally, by documenting emotional face processing skills in PD in a variety of task-processing conditions, we sought to compare these abilities in the visual modality with data on how the same patients understand communicative displays through emotional speech tone (prosody) [55], for which there is more uniform evidence of processing deficiencies associated with early PD [51], [55].

Section snippets

Subjects

Participants were 21 individuals with idiopathic PD and 21 healthy individuals matched on a one-to-one basis for sex, age, and educational status (see Table 1 for major demographic and clinical features of each group). Subjects in the PD group ranged in age from 51 to 83 years and were recruited through a Self Management Program at the Baycrest Centre for Geriatric Care, Toronto, Canada. Idiopathic PD was confirmed on the basis of accepted motor criteria [22] by a residing neurologist.

Results

Data on emotion expression and facial speech processing abilities in PD were examined in sequence within each task processing condition and then compared to neuropsychological background variables. Table 2 summarizes group performance for key measures of both the emotional and facial speech processing tasks.

Discussion

Models of face recognition have proposed distinct functional components for determining a face's identity, for deriving information about the emotional value of (known or unknown) faces, for deciphering facial speech cues, and for assigning other “visually directed” social attributions to faces [18], [25]. This investigation examined how individuals with Parkinson's disease derive information from unfamiliar human faces, focussing on how they analyze prototypical expressions of emotion and

Acknowledgments

Our thanks to all participants in the study and to Marta Fundamenski, Sarah Addleman-Frankel, Sam Hosseini, and Marlene Ecker for help in data collection and analysis. This research was supported by the Canadian Institutes of Health Research, Institute for Aging (New Investigator and Operating support to M. Pell), and represents an Isabel Silverman Canada International Scientific Exchange Program project, supported by the Saul A. Silverman Family Foundation, Toronto, Canada (to C. Leonard).

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