Apathy and Depression Among People Aging With Traumatic Brain Injury: Relationships to Cognitive Performance and Psychosocial Functioning
Publication: The Journal of Neuropsychiatry and Clinical Neurosciences
Abstract
Objective:
Apathy and depression are both common after moderate to severe traumatic brain injury (TBI) and may be especially important to distinguish in older adults with TBI. The authors examined apathy and depression in relation to cognitive performance domains and their potentially unique contribution to psychosocial functioning in this patient population.
Methods:
A total of 106 participants (mean±SD age=64±8 years) with chronic moderate to severe TBI (≥1 year) completed questionnaires assessing severity of apathy (Frontal Systems Behavior Scale–apathy subscale) and depression (Geriatric Depression Scale–15) symptoms, health-related quality of life (HRQoL), and societal participation. Participants also completed neuropsychological tests of episodic memory, processing speed, and executive functioning.
Results:
Apathy symptom severity was significantly associated with all cognitive performances in correlations adjusted for the familywise error rate; a relationship with executive functioning remained after controlling for demographic and injury variables. Depression symptom severity was not significantly associated with cognition after statistical correction. Both symptomatologies uniquely contributed to HRQoL. Only depression symptoms contributed to societal participation. On the basis of clinical cutoffs, half the sample had neither depression nor apathy, approximately 25% met criteria for only apathy, and 25% had both apathy and depression. The combined presence of clinical depression and apathy was associated with worse HRQoL and societal participation.
Conclusions:
This is the first study to examine apathy and depression in relation to cognition and psychosocial functioning in an older sample with a history of TBI. Findings suggest that the two syndromes can be dissociated in clinically meaningful ways, which may help to refine psychiatric and behavioral interventions in this vulnerable population.
Traumatic brain injury (TBI) is a global epidemic, with incidence estimates as high as 69 million cases annually (1). Psychiatric problems are frequently encountered after TBI and can contribute to chronic functional disability (2). Symptoms of two related psychiatric syndromes, apathy and depression, are especially common after moderate to severe forms of TBI and may be difficult to differentiate clinically (3). Given the increased prevalence of apathy with advancing age in the general population (4), older adults with chronic TBI (i.e., individuals aging with a history of moderate or severe TBI) may be particularly at risk for experiencing comorbid apathy and depression and their associated psychosocial consequences.
As a clinical disorder, depression is characterized by low mood or a lack of pleasure or interest in life activities (i.e., anhedonia), often with accompanying symptoms such as sleep and appetite disturbances and difficulties in concentration (5). Apathy refers to reduced goal-directed behavior resulting from diminished motivation, initiation, and planning, ultimately manifesting clinically as a lack of interest, emotion, or concern in life activities (6). Thus, the observable aspects of apathy and depression can be challenging to parse via clinical assessment (e.g., anhedonia in depression vs. a lack of interest resulting from reduced motivation in apathy), leading some to regard apathy as a symptom of depression (7). However, apathy has long been recognized as a separate clinical syndrome (8), and it is often seen among older adults without clinical depression (9). That is, individuals may experience relatively euthymic mood states but nonetheless exhibit reduced interest or drive to engage in activity.
Studies of typical and pathological aging have proposed both overlapping and distinct features of apathy and depression. For example, both are associated with disruptions in functional connectivity between frontostriatal and limbic regions (10), although apathy may be particularly related to brain regions involved in processing the salience of stimuli (11, 12). Depression among older adults is often secondary to chronic medical conditions and life changes and is not necessarily the direct result of the physiological aging process (13). By contrast, observed age-related increases in the prevalence of apathy (4) could be attributed in part to brain changes that preferentially affect the frontal and temporal lobes in older adults (14). The extent to which apathy and its neurobiological correlates are part of the “typical aging” spectrum, however, is unclear, and apathy has been most extensively studied as a symptom of age-related neurodegenerative disease.
Both apathy and depression may affect cognitive functioning, although not necessarily in the same way or to similar degrees. Depression can contribute adversely to cognitive test performance by biasing or distorting thought processes (e.g., directing focus toward negatively valenced information) and ultimately diminishing cognitive effort (15). However, across studies of aging and age-related dementias, apathy symptoms often show stronger relationships than depression symptoms with cognitive performance measures (8, 16)—particularly on tests of executive functioning (17, 18), which may reflect deficits in goal-directed processing. An association between apathy and cognition is supported neuropsychologically, with disruptions to frontal-subcortical circuitry giving rise to both executive deficits and apathy in aging (19). Furthermore, studies have demonstrated, above and beyond the effects of depression, an association between apathy and an increased risk for dementia among older adults (for a review, see 20) as well as poorer subjective quality of life in both clinical and nonclinical samples (21, 22). This suggests that, to some extent, the downstream cognitive and psychosocial consequences of apathy and depression may be independent.
There is evidence to suggest that apathy and depression are also separable clinical entities among individuals with TBI (23, 24). A recent cluster analysis of the Beck Depression Inventory–II among Japanese individuals with chronic TBI of mixed severity revealed clusters of symptoms related to loss of self-worth, interest, energy, and concentration that were selectively associated with self-report on an independent apathy scale (25). Other clusters, labeled by the authors as “somatic” and “affective” depression features, were not significantly related to apathy. Moreover, apathy, but not depression, symptoms predicted daily activity involvement. In a study of severe TBI conducted in Italy, the authors observed that apathy, but not depression, was negatively associated with cognitive flexibility (26), although it was not an explicit goal of the study to differentiate apathy from depression. Overall, joint examination of apathy and depression in relation to cognitive and psychosocial functioning after TBI has been limited. Importantly, previous study samples included individuals across the adult lifespan, with little representation of older adults, for whom distinguishing between apathy and depression may be most challenging and most consequential vis-à-vis psychosocial outcomes. This information could critically inform monitoring of functional status and rehabilitation efforts for a particularly vulnerable population: individuals aging with chronic TBI.
In the present study, we evaluated the extent to which apathy and depression reflected unique symptom constellations among older adults with moderate to severe TBI. Our principal research questions were as follows: Are apathy and depression symptom severities differentially related to cognitive functioning? Do apathy and depression symptom severities make independent contributions to psychosocial functioning? Is the combined presence of clinically significant apathy and depression associated with especially poor psychosocial functioning? Based on findings from studies evaluating non-TBI samples, we hypothesized that apathy would show stronger relationships than depression to cognitive functioning. Testing the hypothesis that apathy and depression symptoms are distinct among people with TBI, we predicted that there would be unique contributions of each symptomatology to key psychosocial outcomes, including health-related quality of life (HRQoL) and societal participation. Additionally, we anticipated that the presence of clinically significant apathy and depression together would result in poorer psychosocial functioning than apathy or depression alone.
Methods
Participants
Participants were adults ages ≥50 years enrolled in a two-center study on aging with TBI. Eligibility criteria included having sustained TBI at least 1 year before study entry that was at least of moderate (including radiologically defined moderate, i.e., “complicated mild”) severity in accordance with National TBI Model Systems criteria (27). Individuals were excluded if they had a history of other neurological or serious psychiatric disorders, such as schizophrenia or bipolar disorder. Of 120 total participants, individuals with motor or sensory impairments that interfered with their ability to complete the behavioral assessment or who were otherwise unable to tolerate assessment procedures were excluded (N=2; one individual with an existing dementia diagnosis and one who was nonverbal). Seven individuals had not been assessed for apathy, which was a later addition to the protocol, and were also excluded. Other exclusions included one individual who had missing depression data and four individuals who were missing at least one cognitive performance measure. Missing data were nonsystematic in nature (e.g., session time limitations). A final sample of 106 participants with a complete data set were entered into the analyses.
Procedure
Study procedures were approved by the institutional review boards of Pennsylvania State University (University Park, Pa.) and Moss Rehabilitation Research Institute (Elkins Park, Pa.) and were consistent with ethical guidelines for human subjects research. Recruitment and study visits occurred between March 2018 and March 2020. Available acute injury information was abstracted from medical records at study enrollment. All study measures were administered during a single session in an outpatient research laboratory. Participants were compensated for their time.
Demographic and Injury Variables
The following variables were collected from each participant at enrollment: age, biological sex, self-identified race, and years of education. Injury chronicity was defined as the number of years from the injury date to the date of study evaluation. Injury severity was classified according to criteria from the U.S. Veterans Affairs TBI Model Systems that consider the most severe acute clinical indicator available (28). To retain maximal resolution in the injury severity variable, analyses included complicated mild, moderate, and severe TBI subgroups.
Primary Measures
Apathy.
The self-report version of the Frontal Systems Behavior Scale (FrSBe) (29) was used to characterize the level of neurobehavioral symptomatology along multiple dimensions (apathy, disinhibition, and executive dysfunction) and exhibits good reliability and validity across samples of patients with neurological disorders (29, 30). The FrSBe apathy subscale consists of 14 items rated on a 5-point scale (1, “almost never”; 2, “seldom”; 3, “sometimes”; 4, “frequently”; and 5, “almost always”) and is a recommended tool for assessing apathy in TBI (31). Apathy scores were converted to sex-, age-, and education-corrected T scores according to norms provided by the scale publisher, where higher scores indicate greater dysfunction (mean±SD T score=66.5±17.8). In accordance with the scale manual, clinically significant apathy was defined as a T score ≥65.
Depression.
The 15-item Geriatric Depression Scale (GDS-15) (32) is an internationally used, well-validated measure of depression symptoms in older adults. Each item response is a binary endorsement (yes or no) of a symptom over the past week, with a possible total score range of 0–15. Three items of the GDS-15 are thought to reflect apathy symptoms (“dropped activities and interests,” “prefer to stay at home,” and “lack of energy”). To determine whether these items should be excluded from the calculation of the total GDS-15 score for maximal separation between constructs, we set an a priori criterion of r<0.7 for the association between the summed GDS-15 apathy items and the FrSBe apathy score. The observed correlation fell below this threshold (0.53), and thus the GDS-15 total score was retained as our depression measure (mean=3.28±3.2). Per guidance from the scale developers, clinically significant depression was defined as a GDS-15 total score ≥5.
Other Clinical Measures
Descriptive statistics for the measures described below are provided in Table S1 in the online supplement .
Cognitive performance.
Neuropsychological tests comprising each cognitive domain are described in detail below. All test scores were age-corrected on the basis of their respective test publisher norms (T and scaled scores), transformed into equivalent z scores, and averaged to yield composite domain scores.
Episodic memory.
Delayed recall trials from the Hopkins Verbal Learning Test–Revised (HVLT-R) (33) and the story recall subtest of the Repeatable Battery for the Assessment of Neuropsychological Status (RBANS) (34) were used as measures of memory functioning. Both tests evaluate verbal episodic memory: the HVLT-R is a word list-learning paradigm evaluating list recall after a 25-minute delay, and the RBANS story recall assesses narrative memory after approximately a 10-minute delay. Both the HVLT-R and RBANS measures are psychometrically validated for use in individuals with moderate to severe TBI (35, 36).
Processing speed.
The processing speed index (PSI) from the Wechsler Adult Intelligence Scale–IV (37) was used as a composite measure of processing speed. The PSI summarizes performance across two speeded tests: coding (digit-symbol substitution) and symbol search (visual search and matching). The tests evaluate visuomotor attention and speed and have been shown to be sensitive to the effects of moderate to severe TBI (38).
Executive functioning.
The following two measures from the Delis-Kaplan Executive Function System (39) were used to index executive functioning: the letter fluency condition of the verbal fluency test and the inhibition condition of the color-word interference (CWI) test. Letter fluency involves speeded word generation to a letter cue and is thought to reflect executive abilities broadly, including self-initiation, self-monitoring, updating, and inhibition (40). The CWI inhibition test is a version of the classic Stroop procedure evaluating prepotent response inhibition. Both of these executive functioning paradigms have demonstrated sensitivity to moderate to severe TBI (41, 42).
HRQoL.
The Quality of Life after Brain Injury (QOLIBRI) questionnaire (43) probes HRQoL among survivors of TBI across six domains (cognition, self-concept, independence in daily life activities, social relationships, emotional functioning, and physical functioning). The QOLIBRI yields a total score summarizing HRQoL and provides information distinct from emotional or functional status (possible scores range from 0 to 100, with higher scores indicating better HRQoL) (44).
Societal participation.
The Participation Assessment with Recombined Tools–Objective (PART-O) (45) is a self-report measure of societal participation level and frequency that was initially validated among persons with TBI and has since been utilized in both clinical and nonclinical samples. Scoring is based on the mean scores for items in each of three domains (productive activity, community activity, and social relations), which, in turn, are averaged to yield the PART-O total score (possible scores range from 0 to 5, with higher scores indicating greater societal involvement).
Statistical Analysis
Associations of apathy and depression symptom severities with the three cognitive scores were initially examined with zero-order correlations (Pearson’s r), correcting for a familywise error rate of 0.05. The associations that remained were evaluated further via residual-effect estimates (partial eta [ηp], a measure of partial correlation [46]), with analyses controlling for the following demographic and injury variables: age, sex, race, years of education, injury severity, and injury chronicity. Potential unique contributions of apathy and depression symptoms to psychosocial functioning (HRQoL and societal participation) were examined by using two linear regression models controlling for demographic and injury variables. Analysis of covariance (ANCOVA) models were used to assess differences in psychosocial functioning between groups with clinically defined apathy, depression, or both. Post hoc pairwise comparisons were performed by using Tukey’s tests to adjust for multiple comparisons. Regression and ANCOVA models were checked for normality (Shapiro-Wilk test) and homoskedasticity (Levene’s test) and passed standard thresholds (all p values >0.05). Statistical analyses were performed in jamovi, version 1.2.27 (47), and R (48) and evaluated significance at an alpha of 0.05. Effect sizes were interpreted in the following manner: correlations <0.3 were defined as small effects, correlations ≥0.3 to <0.7 were defined as medium effects, and correlations ≥0.7 were defined as large effects.
Results
Demographic characteristics of the sample are provided in Table 1. As expected, the correlation between reported severity of apathy and depression symptoms indicated a large effect (r=0.70, p<0.001).
| Characteristic | Value | |
|---|---|---|
| | Mean | SD |
| Age (years) | 63.9 | 8.2 |
| Education (years) | 13.5 | 2.6 |
| | N | % |
| Sex | | |
| Female | 30 | 28 |
| Male | 76 | 72 |
| Race (self-identified) | | |
| Black/African American | 27 | 25 |
| White | 79 | 75 |
| Acute neuroimaging | | |
| Yes | 96 | 91 |
| No | 9 | 8 |
| Unknown | 1 | 1 |
| Injury severity (overall) | | |
| Complicated mild | 17 | 16 |
| Moderate | 24 | 23 |
| Severe | 65 | 61 |
| | Median | Range |
| Injury chronicity (years) | 10.5 | 1.2–31.6 |
| Glasgow Coma Scale scorea | 14 | 3–15 |
| Posttraumatic amnesia (days)b | 15 | 0–77 |
| Time to follow commands (days)c | 0.5 | 0.5–30 |
a
Higher scores indicate less severe injury. Values are based on 83 participants with valid data.
b
Values are based on 88 participants with valid data.
c
Values are based on 85 participants with valid data.
Relationships With Cognitive Performance
Zero-order correlations of apathy and depression with cognitive scores are provided in Table 2. There were small to medium effects between apathy and all cognitive performances that remained significant after correction for the familywise error rate. The only significant effect involving depression (with episodic memory) did not survive adjustment. A significant small effect between apathy and executive functioning was observed when controlling for demographic and injury variables. Relationships involving apathy and the other cognitive performance domains were no longer significant after analyses controlled for these variables.
| Cognitive domain | Frontal Systems Behavior Scale–apathy subscale score | Geriatric Depression Scale–15 score | ||||
|---|---|---|---|---|---|---|
| r | p | ηp | p | r | p | |
| Episodic memory | −0.25 | 0.01b | 0.08 | 0.43 | −0.21 | 0.03 |
| Processing speed | −0.28 | 0.004b | 0.14 | 0.17 | −0.15 | 0.12 |
| Executive functioning | −0.31 | 0.001b | 0.26 | 0.009 | −0.14 | 0.16 |
a
Boldface values indicate significance at an alpha of 0.05. Values of r (with its associated p value) represent the zero-order correlation. Values of ηp (with its associated p value) represent the absolute-value residual effect size with control for demographic and injury variables.
b
Significant after adjustment for a familywise error rate of 0.05 among all zero-order correlations.
Contributions to Psychosocial Functioning
Regression results for psychosocial variables are provided in Table 3. After adjustment for demographic and injury variables, apathy (small effect) and depression (large effect) made significant unique contributions to HRQoL. Only depression made a significant contribution to societal participation (small effect).
| Variable | Health-related quality of life | Societal participation | ||||||
|---|---|---|---|---|---|---|---|---|
| | b | 95% CI | β | ηp2 | b | 95% CI | β | ηp2 |
| Age (years) | −0.08 | −0.33, 0.17 | −0.04 | 0.004 | −0.03*** | −0.04, −0.01 | −0.32 | 0.112 |
| Sex (female=1, male=0) | 1.92 | −2.56, 6.40 | 0.12 | 0.007 | −0.06 | −0.33, 0.21 | −0.09 | 0.002 |
| Race (Black/African American=1, White=0) | 1.71 | −2.93, 6.35 | 0.10 | 0.006 | −0.14 | −0.42, 0.14 | −0.21 | 0.010 |
| Education (years) | −0.19 | −1.01, 0.63 | −0.03 | 0.002 | 0.08** | 0.03, 0.13 | 0.28 | 0.085 |
| Injury severityb | | | | 0.001 | | | | 0.019 |
| Moderate=1 | 1.16 | −5.29, 7.61 | 0.07 | | 0.10 | −0.29, 0.49 | 0.15 | |
| Severe=2 | 0.86 | −4.84, 6.55 | 0.05 | | −0.10 | −0.44, 0.25 | −0.14 | |
| Injury chronicity (years) | −0.15 | −0.52, 0.21 | −0.05 | 0.007 | −0.01 | −0.03, 0.01 | −0.06 | 0.005 |
| FrSBe apathy subscale | −0.23** | −0.39, −0.07 | −0.25 | 0.079 | 0.00 | −0.01, 0.01 | 0.00 | 0.000 |
| GDS-15 | −3.28*** | −4.15, −2.42 | −0.64 | 0.373 | −0.06* | −0.11, −0.01 | −0.28 | 0.051 |
| R2, adjusted R2 | 0.66, 0.63 | | | | 0.27, 0.21 | | | |
| | F | df | p | ηp2 | F | df | p | ηp2 |
| Overall model | 21.11 | 9, 96 | <0.001 | 0.664 | 4.03 | 9, 96 | <0.001 | 0.274 |
a
b=unstandardized regression coefficients; β=standardized regression coefficients; FrSBe=Frontal Systems Behavior Scale; GDS-15=Geriatric Depression Scale–15 item.
b
Complicated mild traumatic brain injury was the reference group (coded 0).
*p<0.05, **p<0.01, ***p<0.001.
Prevalence of Clinically Significant Apathy and Depression
When apathy and depression were considered separately, 53 individuals (50%) endorsed clinically significant apathy, and 28 individuals (26%) endorsed clinically significant depression. When apathy and depression were considered together, 51 individuals (48%) did not endorse either set of symptoms at clinically significant levels. Twenty-seven individuals (26%) reported significant apathy (without depression), and 26 (25%) reported significant apathy and depression. Only two individuals (2%) endorsed significant depression without apathy; we excluded this group from subsequent analyses because of the group’s small size.
Psychosocial Functioning by Clinical Group
ANCOVA models controlling for demographic and injury variables resulted in a significant omnibus effect of clinical group (apathy, depression, or both) on HRQoL (large effect). All post hoc pairwise comparisons were significant with medium to large effects (Table 4 and Figure 1A). ANCOVA for the societal participation variable revealed a small, but significant, effect of clinical group. There was a significant medium effect of poorer societal participation in the group with both apathy and depression relative to the group without either syndrome (Table 4 and Figure 1B).
| Variable | | Health-related quality of life | Societal participation | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| | df | Sum of squares | Mean squares | F | p | ηp2 | Sum of squares | Mean squares | F | p | ηp2 |
| Overall model | 9 | 13,360.29 | 1,484.48 | 10.77 | <0.001 | | 11.01 | 1.22 | 3.77 | <0.001 | |
| Residuals | 94 | 13,289.36 | 141.38 | | | | 34.47 | 0.37 | | | |
| Age (years) | 1 | 0.48 | 0.48 | 0.00 | 0.95 | 0.000 | 4.10 | 4.10 | 11.19 | 0.001 | 0.106 |
| Sex | 1 | 76.64 | 76.64 | 0.54 | 0.46 | 0.006 | 0.03 | 0.03 | 0.09 | 0.77 | 0.001 |
| Race | 1 | 3.43 | 3.43 | 0.02 | 0.88 | 0.000 | 0.42 | 0.42 | 1.15 | 0.29 | 0.012 |
| Education (years) | 1 | 0.00 | 0.00 | 0.00 | 0.998 | 0.000 | 2.87 | 2.87 | 7.82 | 0.006 | 0.077 |
| Injury severity | 2 | 26.07 | 13.03 | 0.09 | 0.91 | 0.002 | 0.62 | 0.31 | 0.85 | 0.43 | 0.018 |
| Injury chronicity (years) | 1 | 74.79 | 74.79 | 0.53 | 0.47 | 0.006 | 0.10 | 0.10 | 0.27 | 0.61 | 0.003 |
| Clinical group | 2 | 13,178.87 | 6,589.44 | 46.61 | <0.001 | 0.498 | 2.86 | 1.43 | 3.91 | 0.02 | 0.077 |
| Post hoc comparisons | df | Mean difference | t | pTukey | Cohen’s d | 95% CI | Mean difference | t | pTukey | Cohen’s d | 95% CI |
| A−/D− vs. A+/D− | 94 | 8.21 | 2.71 | 0.02 | 0.69 | 0.18, 1.21 | 0.18 | 1.13 | 0.50 | 0.29 | −0.22, 0.80 |
| A−/D− vs. A+/D+ | 94 | 28.42 | 9.61 | <0.001 | 2.39 | 1.79, 2.99 | 0.42 | 2.79 | 0.02 | 0.70 | 0.19, 1.20 |
| A+/D− vs. A+/D+ | 94 | 20.21 | 6.03 | <0.001 | 1.70 | 1.09, 2.31 | 0.25 | 1.44 | 0.32 | 0.41 | −0.16, 0.97 |
a
A–=absence of clinically significant apathy; A+=presence of clinically significant apathy; D–=absence of clinically significant depression; D+=presence of clinically significant depression. Boldface values indicate significance at an alpha of 0.05, and pTukey values are Tukey-corrected p values.
FIGURE 1. Psychosocial functioning by clinical group in a sample of older adults with chronic moderate to severe traumatic brain injurya
aPanel A shows participants’ health-related quality of life (HRQoL), and panel B shows participants’ societal participation across clinical groups defined by presence and absence of clinically significant apathy and depression. PART-O=Participation Assessment with Recombined Tools–Objective; QOLIBRI=Quality of Life after Brain Injury questionnaire.
Potential Non-TBI Sources of Apathy
Although participants with diagnosed neurodegenerative diseases or dementia were not included in the sample, apathy may be a prodromal symptom of neurodegenerative disease (49), particularly among those at increased genetic risk. We removed from our analyses nine individuals with clinically significant apathy who reported a history of neurodegenerative disease or dementia, which resulted in comparable effect sizes for associations between apathy and cognitive performance. We also continued to observe a unique contribution of apathy to HRQoL. Therefore, confounding alone cannot explain our observations, and our interpretations are based on the full sample.
Discussion
Apathy and depression are related clinical syndromes; however, they do not show consistent interrelationships across neurological disorders (8, 50), suggesting that they reflect distinct syndromes. The present study examined apathy and depression in a sample of older adults with chronic moderate to severe TBI, who may be particularly susceptible to the effects of both phenomena after injury, to reveal potential dissociations. As expected, the two symptomatologies were highly correlated but exhibited distinct relationships with cognitive and psychosocial functioning.
We found some support for the hypothesis that among older adults with chronic TBI, apathy is more strongly related than depression to cognitive functioning. This was observed even in the context of a high correlation between apathy and depression symptoms. Some relationship between depression and cognition would not have been unexpected, given the well-documented influence of emotional functioning on cognitive performance in many populations, including among individuals with TBI (51). However, the relationships between depression and cognition in our study were not only weak, but they were nonsignificant after correction for multiple comparisons. By contrast, significant (though modest) correlations were observed between apathy and all three cognitive domains assessed (episodic memory, processing speed, and executive functioning).
Consistent with the literature linking apathy to frontal lobe injury (52), the relationship between apathy and cognition may be specific to executive functioning, seeing as this was the only relationship that remained after controlling for demographic and injury characteristics. Our observations are also in line with the proposal that motivated behavior arises from cognitive-control processes, such as decision making, goal maintenance, and outcome monitoring, all of which are supported by frontal-subcortical networks, heavily implicating the medial frontal and prefrontal cortices (12). Damage to these cortical regions and, especially, white matter tracts comprising these networks is commonly implicated in moderate to severe TBI and is associated with executive impairment in addition to social dysfunction and apathy (often grouped together as “dysexecutive syndrome” [53]), providing a neuroanatomical basis for the relationship between apathy and cognitive performance in our study. Although supported by previous literature, these interpretations await empirical testing via neuroimaging and network neuroscience, which may be instructive in elucidating relationships between apathy and cognition (as well as dissociations with depression-related network changes) in chronic TBI. Finally, there may be prognostic implications of a relationship between apathy and cognition: research with older adults demonstrates that the presence of apathy is predictive of later cognitive decline and dementia (54). Because the mechanisms underlying apathy and other symptoms in neurodegenerative dementias are likely manifold (e.g., related to genetic, environmental, or lifestyle risk factors), it remains to be determined whether TBI-related apathy, specifically, is an indicator of later cognitive decline.
In the present study, we also examined depression and apathy in relationship to psychosocial outcomes, including HRQoL and societal participation. In our evaluation of both symptom severity and clinically significant levels of apathy and depression, we found support for the hypothesis that the two phenomena make distinct contributions to psychosocial functioning. Consistent with previous research (55–57), regression models revealed a large effect of depression symptom severity on HRQoL. Although there is little research examining apathy among persons living with chronic moderate to severe TBI, research in uninjured older adult samples suggests that apathy is associated with an increased risk of poor well-being. Similarly, our findings revealed a small, but unique, contribution of apathy symptom severity to HRQoL. Given that HRQoL encapsulates a broad construct, there may be variability between different areas of HRQoL among individuals with TBI, with apathy potentially related to specific patterns of health satisfaction. This is contrasted with depression, which appears to have a pervasive effect on HRQoL. Additionally, our analyses examined the unique effect of apathy on overall HRQoL, after accounting for demographic and injury-related factors as well as depression. In this context, it is not surprising that apathy made a relatively small contribution to overall HRQoL. Moreover, apathy and depression appear to have additive effects, as individuals endorsing both symptomatologies at clinically significant levels reported the poorest HRQoL. These findings argue against apathy being merely a subset of the depression symptom constellation in older adults with chronic TBI.
In regression modeling, societal participation was significantly associated with depression symptom severity but not apathy symptom severity, although both symptomatologies showed some association with societal participation in analyses of clinical subgroups. The association between societal participation and depression among individuals with moderate to severe TBI has been reported previously, with higher levels of participation predicting fewer depression symptoms longitudinally from 1 to 5 years after moderate to severe TBI (58). Participation levels have been shown to vary across the lifespan, related to shifting social roles as individuals age, and the relationship between depression and societal participation may also change across the lifespan. For example, one study of community-dwelling adults 5 years after TBI found that individuals over 65 years old reported lower levels of societal participation than younger age groups. Although clinically significant depression symptoms were associated with worse societal participation among younger individuals, there was no association among those over 65 years old in that study (59). In contrast, we found an association between depression and societal participation in our sample of older adults. There are methodological differences between the present study and previous studies that may account for this discrepancy. Our sample included individuals as young as 50 years old, with a mean age of 64 years for the entire sample, whereas the previous study found a lack of association between depression and societal participation only among individuals over 65 years old (59). Additionally, we used a measure specifically designed for assessing depression among older adults, which may have been more sensitive to depression in this subpopulation.
It is noteworthy that depression symptom severity contributed modestly to societal participation, unlike its large contribution to HRQoL. Furthermore, and contrary to expectations, we did not find apathy symptom severity to be significantly related to societal participation. This observation is inconsistent with previous evidence showing that apathy hinders social and community involvement among both clinical and nonclinical older adult samples (60, 61). Recent research in chronic TBI has demonstrated that a combination of age and injury chronicity (i.e., time elapsed since injury) contributes to disproportionate disability, including participation decrements, among older adults relative to their younger counterparts (62). In this context, there may be systemic problems associated with the overlap of aging and chronic TBI that bear on participation level more strongly than any singular neuropsychiatric factor. It is important to note that this interpretation does not rule out a specific role for apathy or depression in participation challenges. Indeed, when symptoms were discretized in post hoc analyses, individuals with both clinically significant apathy and depression showed reduced societal participation compared with those with neither significant apathy nor depression, suggesting that apathy and depression above threshold levels may be detrimental to societal participation. Nonetheless, we highlight the need for comprehensive modeling of health factors, including health-by-environment interactions, to capture the complexity of aging with TBI.
The present study has important limitations that reveal opportunities for future research. Although our sample size was sufficient for providing a preliminary characterization of this unique population, it did not allow us to further granularize effects by age subgroups. Our study was also observational and cross-sectional, limiting inferences that can be made about causality or symptom trajectories. A strength of our study is that we were able to clinically distinguish between apathy and depression symptoms via self-reports that are easily acquirable in clinical contexts. However, collateral and clinician assessment of apathy may help to further distinguish these constructs and their clinical correlations, particularly in the context of brain injury–related deficits in symptom awareness. Larger samples and longitudinal designs are required to understand how apathy and depression may uniquely or synergistically contribute to psychosocial functioning across later life, including potentially meaningful individual differences that may inform risk identification and treatment. Relatedly, although all participants in this study had sustained only a single moderate to severe TBI, their mild TBI history was not available. Milder injuries, particularly repetitive injuries, may also lead to significant long-term neuropsychiatric consequences and should be investigated as potential predisposing factors for apathy and depression. We used theoretically motivated cognitive composite scores for memory and executive functioning, allowing us to reduce measurement error and limit statistical comparisons. Unlike their component measures, however, the psychometrics of these composites have not been formally evaluated, and they should not be considered comprehensive indices of ability in each domain. Our evaluation of societal participation, although performed with a well-validated instrument for the TBI population, does not reflect the full complexity of this psychosocial outcome. Future work would benefit from examining not only participation frequency but also the personal meaningfulness of participating in activities (i.e., the quality of participation), which may be an especially important aspect of societal participation to older adults.
Conclusions
Consistent with observations in typical and pathological aging, findings from the present study support the distinctiveness of apathy and depression among older adults with chronic moderate to severe TBI, with apathy more closely linked to neurocognitive functioning. Clinically significant levels of both phenomena appear to be common in this population, and each may have potentially unique implications for psychosocial outcomes, particularly subjective quality of life. This highlights the importance of targeted clinical evaluation of both symptomatologies among these individuals to better capture and mitigate sources of psychosocial difficulty. Examining longitudinal symptom trajectories and interrelationships may prove to be instructive in future work. Given the implications of apathy and depression for community functioning, there also exists a need to understand how sociocultural factors may modify the expression and psychosocial effects of these distinct neuropsychiatric symptom constellations within groups and individuals.
Acknowledgments
The authors thank Frank Hillary, Ph.D., for study guidance and review. The authors also thank Rachael Riccitello, B.A., and Roberto Wingfield, B.A., for their contribution to data collection and management.
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Information & Authors
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Received: 10 May 2023
Revision received: 19 December 2023
Accepted: 7 January 2024
Published online: 9 May 2024
Published in print: Fall 2024
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Competing Interests
The authors report no financial relationships with commercial interests.
Funding Information
Supported by the Pennsylvania Department of Health (grant 4100077082).
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