Understanding facial emotion perception in Parkinson's disease: the role of configural processing

Parkinson's disease (PD) has been frequently associated with facial emotion recognition impairments, which could adversely affect the social functioning of those patients. Facial emotion recognition requires processing of the spatial relations between facial features, known as the facial configuration. Few studies, however, have investigated this ability in people with PD. We hypothesized that facial emotion recognition impairments in patients with PD could be accounted for by a deficit in configural processing. To assess this hypothesis, three tasks were proposed to 10 patients with PD and 10 healthy controls (HC): (i) a facial emotion recognition task with upright faces, (ii) a similar task with upside-down faces, to explore the face inversion effect, and (iii) a configural task to assess participants’ abilities to detect configural modifications made on a horizontal or vertical axis. The results showed that when compared with the HC group, the PD group had impaired facial emotion recognition, in particular for faces expressing anger and fear, and exhibited reduced face inversion effect for these emotions. More importantly, the PD group's performance on the configural task to detect vertical modifications was lower than the HC group's. Taken together, these results suggest the presence of a configural processing alteration in patients with PD, especially for vertical, second-order information. Furthermore, configural performance was positively correlated with emotion recognition for anger, disgust, and fear, suggesting that facial emotion recognition could be related, at least partially, to configural processing.     

Perception and memory for faces in Parkinson's disease

This study investigated face processing abilities in patients with late-onset Parkinson's disease. In the first experiment, the Parkinson's disease patients were impaired on a recognition memory test for unfamiliar faces but showed no deficit relative to controls in recognition memory for words. The Parkinson's disease patients were also impaired at matching different photographs of unfamiliar faces. Experiment 2 revealed that the memory deficit affected recognition of familiar as well as unfamiliar faces and extended the face perception impairment to sex decisions and to the analysis of facial speech. An additional verbal recognition memory test again revealed no significant differences between the performance of the Parkinson's disease and control groups. It is argued that the memory impairment is not accountable for simply in terms of the perceptual deficits, and the problems that the patients experience are discussed in terms of the functional model of face processing put forward by Bruce and Young (Brit. J. Psychol. 77, 305-327, 1986).     

Dopamine boosts memory for angry faces in Parkinson's disease

The influence of emotional context on cognitive operations is of fundamental importance for the evolution of higher cognitive functions and their disturbance in neuropsychiatric disorders. The dopamine pathways projecting to prefrontal cortex and the basal ganglia are assumed to play a major role in such emotion‐cognition interactions. Here we provide evidence for such a role by studying working memory for emotional faces in patients with Parkinson's Disease. We studied 25 patients with Parkinson's disease during their on and off medication states. Faces with emotional expressions (happy, angry, sad, neutral or fearful) were shown and the participants had to remember and later recall the identity of the faces ignoring the expressions. We found that dopaminergic medication enhances working memory for angry faces and suppresses it for sad faces. The results elucidate neurochemical mechanisms for the saliency of threatening information and support cognitive explanations of the antidepressant effects of dopamine. They also suggest a role for dopamine in changing emotional‐cognitive biases rather than as a generic cognitive enhancer. © 2010 Movement Disorder Society.     

Recognition memory for unfamiliar faces in Parkinson's disease: behavioral and electrophysiologic measures

We analyzed event-related potentials (ERPs) and behavioral measurements during a recognition memory task in 15 normal elderly subjects and 15 patients with Parkinson's disease (PD). To elicit ERPs unfamiliar faces were repeated immediately after initial presentation (at lag 0), after one intervening face (at lag 1) or at lag 3. Compared to normal controls, PD patients showed decreased accuracy in recognizing new unfamiliar faces. P170 latency and amplitude were similar between both groups. ERP amplitude between 300 and 500 ms after the stimulus in control subjects showed a positive shift (ERP repetition effect) for lag 0 at all sites and for lag 1 and 3 repetitions at the Fz site, while effects in the PD group were not noted at any site, even for the lag 0 repetition. ERP waveforms for the first presentation of faces in PD patients showed a significant positive shift compared to normal controls. These data suggest intact perception but impaired recognition memory for unfamiliar faces in PD. In addition, recognition memory deficits in PD may result from impairment of comparison of structural representations of presented faces with stored representations of faces known to the observer.     

Face recognition memory and configural processing: a developmental ERP study using upright, inverted, and contrast-reversed faces

The effects of configural changes on faces were investigated in children to determine their role in encoding and recognition processes. Upright, inverted, and contrast-reversed unfamiliar faces were presented in blocks in which one-third of the pictures repeated immediately or after one intervening face. Subjects (8-16 years) responded to repeated faces; event-related potentials were recorded throughout the procedure. Recognition improved steadily with age and all components studied showed age effects reflecting differing maturation processes occurring until adulthood. All children were affected by inversion and contrast-reversal, and face-type effects were seen on latencies and amplitudes of early components (P1 and N170), as well as on later frontal amplitudes. The "old-new" repetition effects (larger amplitude for repeated stimuli) were found at frontal sites and were similar across age groups and face types, suggesting a general working memory system comparably involved in all age groups. These data demonstrate that (1) there is quantitative development in face processing, (2) both face encoding and recognition improve with age, but (3) only encoding is affected by configural changes. The data also suggest a gradual tuning of face processing towards the upright orientation.     

Selective processing of buildings and faces during working memory: the role of the ventral striatum

The ventral striatum seems to play an important role during working memory (WM) tasks when irrelevant information needs to be filtered out. However, the concrete neural mechanisms underlying this process are still unknown. In this study, we investigated these mechanisms in detail. Eighteen healthy human participants were presented with multiple items consisting of faces or buildings. They either had to maintain two or four items from one category (low‐ and high‐memory‐load condition), or two from one category and suppress (filter out) two items from the other category (distraction condition). Striatal activity was increased in the distraction as compared with the high‐load condition. Activity in category‐specific regions in the inferior temporal cortex [fusiform face area (FFA) and parahippocampal place area (PPA)] was reduced when items from the other category needed to be selectively maintained. Furthermore, functional connectivity analysis showed significant reduction of striatal–PPA correlations during selective maintenance of faces. However, striatal–FFA connectivity was not reduced during maintenance of buildings vs. faces, possibly because face stimuli are more salient. Taken together, our results suggest that the ventral striatum supports selective WM maintenance by reduced gating of task‐irrelevant activity via attenuating functional connectivity without increasing task‐relevant activity correspondingly.     

Differential role of dopamine in emotional attention and memory: Evidence from Parkinson's disease

Consistent with the hypothesis that dopamine is implicated in the processing of salient stimuli relevant to the modification of various behavioral responses, Parkinson's disease is associated with emotional blunting. To address the hypothesis that emotional attention and memory are modulated by dopaminergic neurotransmission in Parkinson's disease, we assessed 15 nondemented patients with Parkinson's disease while on and off dopaminergic medication and 15 age‐matched healthy controls. Visual stimuli were presented, and recognition was used to assess emotional memory. Response latency was used as a measure of emotional attention modulation. Stimuli were varied based on valence (pleasant, neutral, and unpleasant) and arousal (high and low) dimensions. Controls had significantly better memory for positive than negative stimuli, whereas patients with Parkinson's disease tested off medication had significantly better memory for negative than positive items. This negativity bias was lost when they were tested while on dopaminergic medication. Reaction times in patients with Parkinson's disease off medication were longer than in healthy controls and, paradoxically, were even longer when on medication. Further, although both healthy controls and patients with Parkinson's disease in the “off” state had arousal‐induced prolongation of reaction time, this effect was not seen in patients with Parkinson's disease on medication. These data indicate that dopaminergic neurotransmission is implicated in emotional memory and attention and suggest that dopamine mediates emotional memory via the valence dimension and emotional attention via arousal. Furthermore, our findings suggest that emotional changes in Parkinson's disease result from the effects of both the disease process and dopaminergic treatment. © 2011 Movement Disorder Society     

Correlates of memory in Parkinson's disease

There is much controversy concerning the incidence and nature of dementia, particularly memory impairment, in the parkinsonian patient. Specifically, a question arises with respect to the relationship of numerous personal, neurological, medication, and disability variables to this memory impairment. We administered a recently developed standardized test of recent memory functions to 53 idiopathic parkinsonian patients undergoing Sinemet treatment. Memory scores were correlated with age, sex, education, marital status, length of illness, age at onset of illness, dosage and time on medication, functional status, and the major symptoms of parkinsonism. Of all factors assessed, only increased bradykinesia correlated consistently and pervasively with impaired memory. Some possible explanations are offered.     

Dose-dependent memory impairment in Parkinson's disease

Variation in plasma dopamine level between the time of original learning and subsequent memory retrieval causes a state-dependent memory impairment in Parkinson's disease. The occurrence of this phenomenon is not related to either progression of disease or duration of therapy, but is more likely to occur with high-dosage levels of levodopa-carbidopa.     

Procedural memory in recent-onset Parkinson's disease

Parkinson's disease is accompanied by cognitive disorders which may affect procedural memory. Procedural memory uses a specific knowledge resource that expresses itself through pre-established acting procedures. The aim of this study was to better define the characteristics of procedural memory, first of all, by trying to determine the level of involvement of that memory in the acquisition process (during learning and/or during procedure maintenance), then by specifying the effect of the type of resource involved (verbal or motor). To achieve this, we compared the mnestic performances of 20 recent-onset parkinsonian patients with those of 20 healthy controls, using two memory tasks with a fixed rule (poetry, visuomotor tracking). Result analysis revealed that parkinsonian patients had more difficulty than controls in learning the two rules, regardless of the material involved. Their deficiencies were often associated with an impairment of executive functions, and the procedural memory problems described in parkinsonian patients are linked to the involvement of these resources in the various tasks.     

Overgeneral autobiographical memory in Parkinson's disease

Autobiographical memory (AM) concerns the ability to remember past events from one's own life and consists of autobiographical knowledge (personal facts) and autobiographical incidents (personal events). The novelty of this research was to assess both personal factual and personal event AM in Parkinson's disease (PD) for specified lifetime periods. An autobiographical fluency task was used in which participants were asked to recall personal events and personal facts from five separate lifetime periods. Previous findings as well the brain regions affected in PD lead to the hypothesis that Parkinson's patients would recall less autobiographical memories especially for the most recent lifetime periods. Sixteen non-demented and non-depressed Parkinson's patients and sixteen age-education-matched controls participated. The results showed a temporal gradient for the recall of personal events in Parkinson's patients as they recalled fewer events for recent time periods. The PD group also had more difficulties in recalling autobiographical events rather than an autobiographical knowledge. The difficulty in recalling autobiographical events was characterized by overgenerality, with PD patients failing to generate specific episodic memories.     

Auditory temporal processing in Parkinson's disease

Previous research has suggested that Parkinson's disease (PD) impairs perceptual acuity in the temporal domain. In the present study, psychophysical tests assessing several aspects of auditory temporal processing were administered to a group of PD patients treated with bilateral subthalamic nucleus (STN) stimulation and to a normal control group. Each patient was tested in three clinical conditions: without treatment, with levodopa therapy, and during STN stimulation. In all three conditions, the patients showed a significant deficit in the detection of very short temporal gaps within noise bursts and in the discrimination between the durations of two well-detectable time intervals (circa 50ms) bounded by two temporally non-contiguous pairs of clicks. However, the patients showed no deficit in the detection of a temporal break produced by a local interval change in an otherwise isochronous sequence of 10 clicks spaced by 50-ms intervals. The latter result contradicts previous suggestions that PD slows down an internal clock or pacemaker involved in the perception of short durations. In this regard, we reinterpret previous evidence. Remarkably, the patients' deficits were not diminished by levodopa therapy; in contrast, STN stimulation slightly improved performance, overall. We tentatively ascribe the deficit observed in the gap-detection test to a dysfunctioning of the auditory cortex, impairing its ability to track rapid fluctuations in sound intensity. We argue that the deficit in the duration-discrimination test is the consequence of an impairment in memory and/or attention rather than in the perception of time per se.     

Reward processing abnormalities in Parkinson's disease

The primary motor cortex is important for motor learning and response selection, functions that require information on the expected and actual outcomes of behavior. Therefore, it should receive signals related to reward. Pathways from reward centers to motor cortex exist in primates. Previously, we showed that gamma aminobutyric acid–A–mediated inhibition in the motor cortex, measured by paired transcranial magnetic stimulation, changes with expectation and uncertainty of money rewards generated by a slot machine simulation. We examined the role of dopamine in this phenomenon by testing 13 mildly affected patients with Parkinson's disease, off and on dopaminergic medications, and 13 healthy, age‐matched controls. Consistent with a dopaminergic mechanism, reward expectation or predictability modulated the response to paired transcranial magnetic stimulation in controls, but not in unmedicated patients. A single dose of pramipexole restored this effect of reward, mainly by increasing the paired transcranial magnetic stimulation response amplitude during low expectation. Levodopa produced no such effect. Both pramipexole and levodopa increased risk‐taking behavior on the Iowa Gambling Task. However, pramipexole increased risk‐taking behavior more in patients showing lower paired transcranial magnetic stimulation response amplitude during low expectation. These results provide evidence that modulation of motor cortex inhibition by reward is mediated by dopamine signaling and that the physiological state of the motor cortex changes with risk‐taking tendency in patients on pramipexole. The cortical response to reward expectation may represent an endophenotype for risk‐taking behavior in patients on agonist treatment. © 2011 Movement Disorder Society     

The role of the striatum in sentence processing: Disentangling syntax from working memory in Huntington's disease

The role of sub-cortical structures in language processing remains controversial. In particular, it is unclear whether the striatum subserves language-specific processes such as syntax or whether it solely affects language performance via its significant role in executive functioning and/or working memory. Here, in order to address this issue, we attempted to equalize working memory constraints while varying syntactic complexity, to study sentence comprehension in 15 patients with striatal damage, namely Huntington's disease at early stage, and in 15 healthy controls. More particularly, we manipulated the syntactic relation between a name and a pronoun while holding the distance between them constant. We exploited a formal principle of syntactic theory called Principle C. This principle states that whereas in a sentence such as "Paul smiled when he entered" Paul and he can be a single person, this interpretation is blocked in sentences such as "He smiled when Paul entered". In a second experiment we varied working memory load using noun-adjective gender agreement in center-embedded and right-branching relatives (e.g., "the girl who watches the dog is green" vs. "the girl watches the dog which is green"). The results show that HD patients correctly establish name-pronoun coreference but they fail to block it when Principle C should apply. Furthermore, they have good performance with both center-embedded and right-branching relatives, suggesting that their difficulties in sentence comprehension do not arise from memory load impairment during sentence processing. Taken together, our findings indicate that the striatum holds a genuine role in syntactic processing, which cannot be reduced to its involvement in working memory. However, it only impacts on particular aspects of syntax that may relate to complex computations whereas other operations appear to be preserved. Hypotheses about the role of the striatum in syntactic processing are discussed.     

Emotional processing in Parkinson's disease: a systematic review

Parkinson's disease provides a useful model for studying the neural substrates of emotional processing. The striato-thalamo-cortical circuits, like the mesolimbic dopamine system that modulates their function, are thought to be involved in emotional processing. As Parkinson's disease is histopathologically characterized by the selective, progressive, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, it can therefore serve as a model for assessing the functional role of these circuits in humans. In the present review, we begin by providing a synopsis of the emotional disturbances observed in Parkinson's disease. We then discuss the functional roles of the striato-thalamo-cortical and mesolimbic circuits, ending with the conclusion that both these pathways are indeed involved in emotional processing.     

Time resolution for visual information processing in Parkinson's disease

It has been suggested that a deficit in timing could be thecause of the sensory disturbances reported for Parkinson's disease. Totest this hypothesis the temporal discrimination thresholds in fourvisual tasks were used to study 45 healthy young people, 14 healthyelderly people, and 17 patients with Parkinson's disease. In thesetasks, subjects watched a computer controlled light emitting diodedisplay and pushed a button when the visual event previously specifiedby the researcher was perceived. The time between successive imagesrequired to discriminate a visual detail was accurately quantified. Intwo of the four tasks, the time for visual processing of imagesequences was longer in the elderly group than in the young group. Nosignificant differences were found between patients with Parkinson'sdisease and their age matched controls for any of the four tasks.Present data show normal temporal discrimination and no slowing in theinitial steps of visual processing in Parkinson's disease.

     

The influence of left and right hemisphere brain damage on configural and featural processing of affective faces

The literature about the lateralization of facial emotion perception according to valence (positive, negative) is conflicting; investigating the underlying processes may shed light on why some studies show right-hemisphere dominance across valence and other studies demonstrate hemispheric differences according to valence. This is the first clinical study to examine whether the use of configural and featural cues underlies hemispheric differences in affective face perception. Right brain-damaged (RBD; n = 17), left brain-damaged (LBD; n = 17) and healthy control (HC; n = 34) participants completed an affective face discrimination task that tested configural processing using whole faces and featural processing using partial faces. No group differences in expression perception according to valence or processing strategy were found. Across emotions, the RBD group was less accurate than the HC group in discriminating whole faces, whilst the RBD and LBD groups were less accurate than HCs in discriminating partial faces. This suggests that the right hemisphere processes facial expressions from configural and featural information, whereas the left hemisphere relies more heavily on featural facial information.     

Dopamine and memory function in Parkinson's disease

Response fluctuations in motor function, complicating long-term dopaminomimetic therapy of Parkinson's disease, may extend to the cognitive realm. To evaluate the effect of levodopa treatment both on attention as well as acquisition and retrieval of memory tasks, parkinsonian patients were examined neuropsychologically both while medicated with levodopa/carbidopa ("on") and when the medication's antiparkinsonian effect had worn off ("off"). Significant cognitive differences emerged only on the delayed recall of complex verbal materials, where patients when "on" performed better compared with their "off" state. Comparison of change scores across states (administration or withholding of levodopa/carbidopa between acquisition and retrieval, "off" to "on" or "on" to "off"), revealed no substantial differences as a function of dopaminomimetic therapy. These results support the view that slight changes in cognition are associated with dopaminomimetic therapy of Parkinson's disease, but that these changes may be task-specific.