Age-related differences in brain activation during emotional face processing
Introduction
Advancing age is associated with significant declines on neurobehavioral tasks that demand substantial mental effort, rely heavily on processing speed, and are characterized by novelty and complexity of the stimuli [36]. Functional neuroimaging techniques, such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), provide roughly ‘real-time’ representation of brain hemodynamic response, and thus enable the in vivo study of neural mechanisms underlying mental processes. Several studies have used functional neuroimaging paradigms to study the neural basis of age-related changes in mental abilities. These investigations have examined episodic memory [10], [11], [12], [26], [33], [46], [48], [67], working memory [32], [51], [64], [66], attention [5], [39], [47], and executive functioning [71]. Generally, the evidence suggests that older adults tend to activate more regions than their younger counterparts. This recruitment of additional cortical regions may reflect an attempt to compensate for cortical networks that have become less efficient in advanced age. Furthermore, functional imaging data suggest that older adults recruit frontal regions when faced with effortful tasks [25], [61]. This effect too can be considered compensatory, in view of evidence for age-associated reduction in frontal lobe volume (e.g. [16], [40], [61], [62]).
Whereas much of aging research has focused on the neurobiologic substrates of cognition, the neural underpinnings of emotion processing in aging have received little attention. Lesion studies aimed at identifying the neural substrates of emotion have implicated the limbic system, particularly the amygdala, as well as cortical areas including the orbitofrontal, dorsolateral prefrontal, parietal, and temporal cortices [1], [2], [4], [13], [17], [18], [21], [34], [45], [65]. Functional neuroimaging studies have used diverse paradigms to examine emotion processing, including emotion discrimination [29], [30], [41], mood induction [24], [59], [68], [69], [70], fear conditioning [44], [52], prosodic identification [9], reward and punishment conditions [42], [57], [80] and viewing of emotionally provocative stimuli [7], [14], [37], [43], [58], [63]. Generally, these studies support the lesion findings that limbic regions, particularly the amygdala, and certain prefrontal regions are consistently involved in emotion processing [29], [30], [31], [53], [54], [55], [72].
Facial expression has been considered a salient component of emotional behavior [19], and the ability to identify and distinguish facial emotion is an important component of emotion processing. The preponderance of data from fMRI studies of activation patterns associated with perception of facial expression in young healthy adults indicate activation of limbic regions, particularly the amygdala, in response to emotional faces [30], [31], [68], [72]. However, inferior frontal regions seem also to be involved in facial emotion discrimination. For example, Sprengelmeyer et al., evaluated activation patterns associated with performance of gender discrimination of faces expressing disgust, fear and anger compared with neutral expressions. They detected left inferior frontal activation for all three emotions, with different patterns for each emotion in other cortical and subcortical regions [72]. Interestingly, it appears that activation of the amygdala may be dependent upon the relevance of the facial emotion itself to the task at hand. For instance, in the aforementioned study, where emotional faces were used but the task required gender discrimination, amygdala activation was not observed [72]. Similarly, Gur et al. [30] observed activation in inferior frontal regions, regardless of the type of facial emotion task, but amygdala and hippocampal activation was modulated by the task relevance of the emotional aspects of the face.
Although the effect of aging on emotion processing has received limited attention, there is evidence to suggest that some deficits, such as “lesser expressivity” are present in older adults [27], [49]. There is also evidence that older adults are more vulnerable than young adults to adverse effects of negative emotional states on memory [20] and other cognitive abilities [56]. Behavioral studies of emotional perception indicate that older adults may perceive emotions less accurately than younger adults. For example, older adults appear to process lexical emotional stimuli less accurately than their younger counterparts [28]. Furthermore, results of a study that required facial expression identification indicate that older adults, when required to identify negative affect, are less accurate than young adults [50].
To our knowledge, only one study has used functional neuroimaging to study emotion processing in older adults. Paradiso et al. [58], used PET to study brain activation in healthy elderly individuals during a mood induction task. Participants watched video clips intended to evoke positive or negative emotions while regional cerebral blood flow was measured. During all conditions, participants activated visual cortices, orbital and medial frontal cortices, and the fusiform gyrus. In the happy condition only, subjects activated the anterior cingulate and entorhinal cortex, while in the disgust condition only, subjects activated the medial thalamus. However, the conclusions about the effect of aging on emotion processing are limited due to the fact that this study looked only at older adults.
The goal of the present study was to examine the influence of age on activation of limbic and cortical regions during facial emotion processing. Regional activation during an emotion-discrimination task was compared to activation during passive baseline and an active control condition requiring discrimination of non-emotional aspects of the same faces. Based on previous studies of emotion discrimination in young, healthy individuals, we expected young participants to show activation in limbic regions (amygdala, hippocampus, parahippocampal gyrus), fusiform cortex, occipital regions, and inferior frontal cortex. The bulk of the functional imaging data suggest that older adults, perhaps in an attempt to compensate for diminished function in other brain regions, tend to recruit frontal regions when faced with effortful tasks (see [10], [25], [61] for review). Thus, we predicted that, due to the decreased efficiency in temporo-limbic regions associated with advancing age, older adults would demonstrate increased use of frontal relative to limbic regions, compared to the younger adults.
Section snippets
Participants
Participants were healthy individuals recruited through advertisements in the local newspapers and in collaboration with the Penn Passcard Program for Healthy Living of the Institute on Aging at the University of Pennsylvania. Participants underwent medical screening to exclude individuals with a history of any illnesses affecting brain function. Specifically, participants were screened for history of neurological and/or psychiatric conditions, head trauma with loss of consciousness,
Performance
For the emotion discrimination task, younger adults were both more accurate (young: 93.2±7.7%; old: 77.1±9.7%, t(11)=3.34, P<0.01) and faster (RT: young 919.5±105.1; old 1200.5±205.9, t(11)=3.18, P<0.01) than the older adults. Performance of the age discrimination task also tended to be more accurate for the young (82.8±4.5%) than for the older adults (72.2±15.0%, t(11)=1.80, P<0.10), although this difference was not significant. In addition, the older adults were significantly slower in their
Discussion
The main finding of this study is that young and older adults activate different cortical networks when processing facial affect. Independent of task demands, young adults activate bilateral prefrontal and visual cortices during the processing of emotional facial expressions. However, when the task demands are for processing the emotional aspects of the facial expressions, young adults also enlist right hemisphere temporo-limbic regions, particularly the amygdala. These findings are congruent
Acknowledgements
The authors thank Norman Butler and the HUP MR technology staff for their invaluable help in data acquisition. We are grateful for the assistance of Jennifer Boyle and the staff of the Penn Passcard Program for Healthy Living of the Institute on Aging for their assistance in participant recruitment. Supported by grants MH60722, MH43880, MH19112, and the Bosworth Fund.
References (80)
How to estimate global activity independent of changes in local activity
NeuroImage
(1997)- et al.
Response and habituation of the human amygdala during visual processing of facial expression
Neuron
(1996) - et al.
Face processing impairments after encephalitis: amygdala damage and recognition of fear
Neuropsychologia
(1998) - et al.
Recognition of emotional prosody and verbal components of spoken language: an fMRI study
Brain Res. Cogn. Brain Res.
(2000) - et al.
Lesion localization in acquired deficits of emotional expression and comprehension
Brain Cogn.
(1990) Emotion in the perspective of an integrated nervous system
Brain Res. Rev.
(1998)- et al.
Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives
Prog. Neurobiol.
(1995) Functional brain imaging and age-related changes in cognition
Biol. Psychol.
(2000)- et al.
Effects of emotional discrimination tasks on cerebral blood flow: regional activation and its relation to performance
Brain Cogn.
(1994) - et al.
Brain activation during facial emotion processing
Neuroimage
(2002)
Age-related shift in brain region activity during successful memory performance
Neurobiol. Aging
A study of analysis parameters that influence the sensitivity of event-related fMRI analyses
Neuroimage
Cortical sites of sustained and divided attention in normal elderly humans
Neuroimage
Neural substrates of facial emotion processing using fMRI
Cogn. Brain Res.
Neuroanatomical correlates of pleasant and unpleasant emotion
Neuropsychologia
Human amygdala activation during conditioned fear acquisition extinction: a mixed-trial fMRI study
Neuron
fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory
Cogn. Brain Res.
Parallel neural responses in amygdala subregions and sensory cortex during implicit fear conditioning
Neuroimage
Functional MRI reveals left amygdala activation during emotion
Psychiat. Res.
Differential effects of mood on cortical cerebral blood flow: a 133 Xenon clearance study
Psychiat. Res.
Mood effects on limbic blood flow correlate with emotional self-rating: a PET study with oxygen-15 labeled water
Psychiat. Res.
Regionally specific cell loss of neurons in the aging human hippocampus
Neurobiol. Aging
Facial expression processing after amygdalotomy
Neuropsychologia
Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala
Nature
Cortical systems for the recognition of emotion in facial expressions
J. Neurosci.
Correction of ghost artifacts and distortion in echo-planar MR imaging with an iterative image reconstruction technique
Radiology
Contribution of the anteromedial temporal lobes to the evaluation of facial emotion
Neuropsychology
The effects of divided attention on encoding- and retrieval-related brain activity: a PET study of younger and older adults
J. Cogn. Neurosci.
Hemispheric asymmetry reduction in older adults: the HAROLD model
Psychol. Aging
Age-related differences in neural activity during item and temporal-order memory retrieval: a positron emission tomography study
J. Cogn. Neurosci.
Age-related differences in effective neural connectivity during encoding and recall
Neuroreport
Event-related activation in the human amygdala associates with later memory for individual emotional experience
J. Neurosci.
Sex differences in aging of the human frontal and temporal lobe
J. Neurosci.
Towards a neuropathology of emotion and mood
Nature
Aging, emotional states, and memory
Am. J. Psychiat.
Neural mechanisms of emotion
J. Consult Clin. Psychol.
Statistical parametric maps in functional imaging: a general linear approach
Hum. Brain Mapp.
Brain activity during transient sadness and happiness in healthy women
Am. J. Psychiat.
Cited by (238)
Changes in functional connectivity associated with facial expression processing over the working adult lifespan
2022, CortexCitation Excerpt :Several studies have examined age differences in neural response to facial expressions, although again, most have tested differences in activation between distinct groups of younger and older adults (e.g., Zsoldos, Cousin, Klein-Koerkamp, Pichat, & Hot, 2016). A common result is that younger adults show higher activation in the amygdala and hippocampus than older adults for facial expressions of emotion, particularly in response to angry and fearful faces (Fischer et al., 2005; Fischer, Nyberg, & Bäckman, 2010; Gunning-Dixon et al., 2003; Iidaka et al., 2002; Keightley, Chiew, Winocur, & Grady, 2007; Tessitore et al., 2005), whereas older adults show higher activation than younger adults in prefrontal areas (Fischer et al., 2010; Gunning-Dixon et al., 2003; Tessitore et al., 2005; Zsoldos et al., 2016). To our knowledge, only one study has examined differences in neural response to facial expressions that occur across the adult lifespan, where participants aged 12–79 were presented fearful, happy, and neutral faces during functional Magnetic Resonance Imaging (fMRI) (Williams et al., 2006).
Are facial emotion recognition tasks adequate for assessing social cognition in older people? A review of the literature
2021, Archives of Gerontology and GeriatricsNo evidence for any effect of multiple sessions of frontal transcranial direct stimulation on mood in healthy older adults
2020, NeuropsychologiaCitation Excerpt :No other previous study has investigated the effect of multiple sessions of TDCS on mood in a healthy older population and an important consideration is the neural changes that come with age. Brain activity patterns are known to be different in older relative to younger adults (Gunning-Dixon et al., 2003; Roalf et al., 2011), and normal aging has been linked to several neural changes that affect plasticity negatively, particularly in hippocampal and frontal regions (Burke and Barnes, 2006; Lövdén et al., 2010). Given the uncertainty concerning the precise neurophysiological mechanism of TDCS, particularly in non-motor areas such as the DLPFC, it is difficult to speculate in how age may affect the physiological response to TDCS (Heise et al., 2014; Horvath et al., 2015).