Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden
Enhanced emotional empathy, the ability to share others’ affective experiences, can be a feature of Alzheimer’s disease (AD), but whether emotional empathy increases in the preclinical phase of the disease is unknown. We measured emotional empathy over time (range = 0 – 7.3 years, mean = 2.4 years)...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2023-01-01
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| Series: | NeuroImage: Clinical |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158222003473 |
| _version_ | 1797869785557499904 |
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| author | Tiffany E. Chow Christina R. Veziris Renaud La Joie Alex J. Lee Jesse A. Brown Jennifer S. Yokoyama Katherine P. Rankin Joel H. Kramer Bruce L. Miller Gil D. Rabinovici William W. Seeley Virginia E. Sturm |
| author_facet | Tiffany E. Chow Christina R. Veziris Renaud La Joie Alex J. Lee Jesse A. Brown Jennifer S. Yokoyama Katherine P. Rankin Joel H. Kramer Bruce L. Miller Gil D. Rabinovici William W. Seeley Virginia E. Sturm |
| author_sort | Tiffany E. Chow |
| collection | DOAJ |
| description | Enhanced emotional empathy, the ability to share others’ affective experiences, can be a feature of Alzheimer’s disease (AD), but whether emotional empathy increases in the preclinical phase of the disease is unknown. We measured emotional empathy over time (range = 0 – 7.3 years, mean = 2.4 years) in 86 older adults during a period in which they were cognitively healthy, functionally normal, and free of dementia symptoms. For each participant, we computed longitudinal trajectories for empathic concern (i.e., an other-oriented form of emotional empathy that promotes prosocial actions) and emotional contagion (i.e., a self-focused form of emotional empathy often accompanied by feelings of distress) from informant ratings of participants’ empathy on the Interpersonal Reactivity Index. Amyloid-β (Aβ) positron emission tomography (PET) scans were used to classify participants as either Aβ positive (Aβ+, n = 23) or negative (Aβ-, n = 63) based on Aβ-PET cortical binding. Participants also underwent structural and task-free functional magnetic resonance imaging approximately two years on average after their last empathy assessment, at which time most participants remained cognitively healthy. Results indicated that empathic concern, but not emotional contagion, increased more over time in Aβ+ participants than in Aβ- participants despite no initial group difference at the first measurement. Higher connectivity between certain salience network node-pairs (i.e., pregenual anterior cingulate cortex and periaqueductal gray) predicted longitudinal increases in empathic concern in the Aβ+ group but not in the Aβ- group. The Aβ+ participants also had higher overall salience network connectivity than Aβ- participants despite no differences in gray matter volume. These results suggest gains in empathic concern may be a very early feature of AD pathophysiology that relates to hyperconnectivity in the salience network, a system that supports emotion generation and interoception. A better understanding of emotional empathy trajectories in the early stages of AD pathophysiology will broaden the lens on preclinical AD changes and help clinicians to identify older adults who should be screened for AD biomarkers. |
| first_indexed | 2024-04-10T00:18:14Z |
| format | Article |
| id | doaj.art-d54b5d91f07e45f0ba7c18f480473d5d |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-04-10T00:18:14Z |
| publishDate | 2023-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-d54b5d91f07e45f0ba7c18f480473d5d2023-03-16T05:03:53ZengElsevierNeuroImage: Clinical2213-15822023-01-0137103282Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burdenTiffany E. Chow0Christina R. Veziris1Renaud La Joie2Alex J. Lee3Jesse A. Brown4Jennifer S. Yokoyama5Katherine P. Rankin6Joel H. Kramer7Bruce L. Miller8Gil D. Rabinovici9William W. Seeley10Virginia E. Sturm11Memory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USA; Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USA; Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USA; Department of Radiology and Biomedical Imaging, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USAMemory and Aging Center, Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, CA 94158, USA; Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, CA 94158, USA; Corresponding author at: University of California, San Francisco, Memory and Aging Center, Box 1207, 675 Nelson Rising Lane, Suite 190, San Francisco, CA 94143, USA.Enhanced emotional empathy, the ability to share others’ affective experiences, can be a feature of Alzheimer’s disease (AD), but whether emotional empathy increases in the preclinical phase of the disease is unknown. We measured emotional empathy over time (range = 0 – 7.3 years, mean = 2.4 years) in 86 older adults during a period in which they were cognitively healthy, functionally normal, and free of dementia symptoms. For each participant, we computed longitudinal trajectories for empathic concern (i.e., an other-oriented form of emotional empathy that promotes prosocial actions) and emotional contagion (i.e., a self-focused form of emotional empathy often accompanied by feelings of distress) from informant ratings of participants’ empathy on the Interpersonal Reactivity Index. Amyloid-β (Aβ) positron emission tomography (PET) scans were used to classify participants as either Aβ positive (Aβ+, n = 23) or negative (Aβ-, n = 63) based on Aβ-PET cortical binding. Participants also underwent structural and task-free functional magnetic resonance imaging approximately two years on average after their last empathy assessment, at which time most participants remained cognitively healthy. Results indicated that empathic concern, but not emotional contagion, increased more over time in Aβ+ participants than in Aβ- participants despite no initial group difference at the first measurement. Higher connectivity between certain salience network node-pairs (i.e., pregenual anterior cingulate cortex and periaqueductal gray) predicted longitudinal increases in empathic concern in the Aβ+ group but not in the Aβ- group. The Aβ+ participants also had higher overall salience network connectivity than Aβ- participants despite no differences in gray matter volume. These results suggest gains in empathic concern may be a very early feature of AD pathophysiology that relates to hyperconnectivity in the salience network, a system that supports emotion generation and interoception. A better understanding of emotional empathy trajectories in the early stages of AD pathophysiology will broaden the lens on preclinical AD changes and help clinicians to identify older adults who should be screened for AD biomarkers.http://www.sciencedirect.com/science/article/pii/S2213158222003473PreclinicalAlzheimer's diseaseSocial cognitionCompassionAnterior cingulate cortexSalience network |
| spellingShingle | Tiffany E. Chow Christina R. Veziris Renaud La Joie Alex J. Lee Jesse A. Brown Jennifer S. Yokoyama Katherine P. Rankin Joel H. Kramer Bruce L. Miller Gil D. Rabinovici William W. Seeley Virginia E. Sturm Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden NeuroImage: Clinical Preclinical Alzheimer's disease Social cognition Compassion Anterior cingulate cortex Salience network |
| title | Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden |
| title_full | Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden |
| title_fullStr | Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden |
| title_full_unstemmed | Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden |
| title_short | Increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid-β burden |
| title_sort | increasing empathic concern relates to salience network hyperconnectivity in cognitively healthy older adults with elevated amyloid β burden |
| topic | Preclinical Alzheimer's disease Social cognition Compassion Anterior cingulate cortex Salience network |
| url | http://www.sciencedirect.com/science/article/pii/S2213158222003473 |
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