Verbal Memory Abilities in Severe Childhood Psychiatric Disorders and the Influence of Attention and Executive Functions
Brian C. Kavanaugh1,2,*, Charles E. Gaudet3, Jennifer A. Dupont-Frechette3, Perrin P. Tellock4, Isolde D. Maher5, Lauren D. Haisley6, Karen A. Holler1,2
Abstract Despite prior adult research regarding the influence of executive functions on memory performance, there has been inconsistent prior research on the role of executive functions on memory performance in children, particularly those children with severe psychiatric disorders. A medical chart review was conducted for 76 children (ages 6–12 years) who received a neuropsychological evaluation during children’s psychiatric inpatient program hospitalization.Aseries of hierarchical regression analyses investigated the role of attention/executive and non-executive functions in verbal memoryperformance (immediate recall, delayed recall, and delayed recognition).Demographic and verbal measureswere entered into blocks 1 and 2 for all analyses, followed by attention and executive functions (i.e., attention span, sustained attention, verbal fluency, cognitive flexibility, inhibitory control, and planning/organization). Nearly 15% of the participants displayed memory impairment. Results of regression analyses indicated attention/executive dysfunction severity predicted overall memory performance. Attention span predicted performance on all three memory conditions. Planning/organization accounted for unique variance in immediate recall condition while inhibitory control accounted for unique variance in delayed recall condition. These results indicate that verbal memory problems frequently occur in severe childhood psychiatric disorders. Further, planning/organization deficits may influence immediate recall, while inhibitory control deficits may influence delayed recall. Alternatively, delayed recognition memory may be the most resistant to the negative influence of executive deficits on verbal memory performance in childhood psychiatric disorders.
Memory is a complex neurocognitive domain that involves the encoding, retaining, and retrieving of information (Schaefer& Hebben, 2014). Due to the complexity of the memory process, effective memory is highly dependent on other neurocognitive domains such as language, attention, processing speed, and executive functions (Baron, 2004; Lezak et al., 2004). Particularly in childhood non-neurologic settings, the effective clinician must consider the integrity of other neurocognitive functions as potential contributors to poor memory performance (Baron, 2004; Lezak et al., 2004). Poor memory performance on standardized neuropsychological measures has been previously identified in childhood psychiatric disorders such as bipolar disorder (Dickstein et al., 2004; Glahn et al., 2005; McClure et al., 2005; Udal, Oygarden, Egeland, Malt,&Groholt, 2012),ADHD(Andersen, Hovik, Skogli, Egeland,&Oie, 2013; Henin et al., 2007; Udal et al., 2012), depressive disorders (Brooks, Iverson, Sherman,&Roberge, 2010; Gunther, Holkamp, Jolles, Herpertz-Dahlmann,&Konrad, 2004; Lauer et al., 1994), psychosis (Udal et al., 2012), and psychiatric comorbidity (Frost, Moffitt, & McGee, 1989). Such studies have evaluated memory with verbal list learning (Andersen et al., 2013; Brooks et al., 2010; Frost et al., 1989; Glahn et al., 2005; Gunther et al., 2004; Henin et al., 2007; Lauer et al., 1994; McClure et al., 2005; Udal et al., 2012), and spatial/figure recognition measures (Brooks et al., 2010; Dickstein et al., 2004), with only one study utilizing a story-format memory measure (McClure et al., 2005). In McClure and colleagues (2005) study, poor story memory performance was identified within the bipolar group in immediate and delayed recall (no administered recognition format). Prior research has provided limited information regarding the specific memory stage that may be impaired in childhood psychiatric disorders (e.g., encoding or retrieval). For example, in one study depression/anxiety disorders were associated with poor delayed recall and recognition, but not immediate recall nor learning curve (Gunther et al., 2004), while in another study depression was associated with poor immediate recall and not delayed recall or learning curve (Lauer et al., 1994). Childhood psychiatric disorders appear to be associated with a non-specific pattern of loweredmemoryperformance, although research on verbalmemory for semantically complex information remains limited.
Childhood psychiatric disorders also frequently display associated deficits in executive functions, a collection of “top-down” control and self-regulatory processes required to obtain goals and objectives (Barkley, 2012; Diamond, 2013). Many of the same studies that identified poor memory functioning in these disorders also identified deficits in executive functions, or the presence of executive dysfunction (Andersen et al., 2013; Brooks et al., 2010; Dickstein et al., 2004; Henin et al., 2007). Given the inherent executive dysfunction in childhood psychiatric disorders (Hale & Fitzer, 2015), it could be hypothesized that poor memory in childhood psychiatric disorders may be largely influenced by executive dysfunction. While two studies evaluated group differences of the presence/absence of ADHD diagnosis/symptoms (Andersen et al., 2013; Henin et al., 2007), none of the studies evaluated the potential influence of executive functions on memory performance. In adult clinical neuropsychology samples, memory and executive abilities have a high degree of clinical overlap (e.g., sequencing/working memory; Duff, Schoenberg, Scott, & Adams, 2005), with poor verbal memory performance identified in patients with executive dysfunction (Hill, Alosco, Bauer, & Tremont, 2012; Tremont, Halpert, Javorsky, & Stern, 2000). Executive measures also account for a large proportion of memory performance variance in adult samples (e.g., complex visual sequencing and set shifting; Hill et al., 2012; Temple, Davis, Silverman, & Tremont, 2006). The pediatric literature remains more limited. While attention/executive functions did not contribute to verbal memory performance in a large, mixed pediatric sample (Jordan, Tyner, & Heaton, 2013), attention/ executive functions (including planning, abstraction, and mental tracking) predicted verbal and visual memory in a pediatric sample of temporal lobe epilepsy (Rzezak, Guimaraes, Fuentes, Geurreiro, & Valente, 2012). In this sample, the severity of executive dysfunction was additionally associated with lowered memory performance. Given the inconsistent research on the neurocognitive contributors to poor memory performance in children, this study sought to examine the verbal memory abilities (i.e., story memory) in a sample of children in an admission to inpatient psychiatric treatment program. This sample is defined as children with severe psychiatric disorders, given the severity of their psychiatric presentation requires themost intensive psychiatric treatment (i.e., inpatient care). This is instead of the more pejorative terms previously used to describe similar groups of children requiring hospitalization (e.g., psychiatrically disturbed inpatients). It was hypothesized that a large portion of the sample would display poor memory abilities (indicated by a high degree of impaired scores) and that memory performance would be predicted by a combination of attention/executive and non-executive (i.e., verbal) domains.
IRB approval was obtained to conduct this medical chart review study. Two-hundred and thirty-eight children consecutively referred for a neuropsychological evaluation at a children’s inpatient psychiatric program within a medical school-affiliated children’s psychiatric hospital were considered for inclusion in the present study. Participants were generally referred for neuropsychological evaluation to characterize neurocognitive functioning and guide treatment planning. The program admits children ages 3–12, although the majority of children referred for neuropsychological evaluation are 6–12 years of age. The inclusion criteria for the present study were 6–12 years of age at the time of the neuropsychological evaluation, sufficient information available in hospital medical records to extract key variables, a diagnosis of at least one psychiatric disorder by a hospital psychiatrist according to DSM-IV-TR or later DSM-5 criteria following psychiatric evaluation as part of the hospitalization (American Psychiatric Association, 2000, 2013), and completion of memory, verbal, and attention/executive measures utilized in the present study. TheWRAML-2 StoryMemory is the primary verbal memory measure administered in the brief neuropsychological battery and thus the only memory measure available for the present study. Seventy-six children met inclusion criteria (out of total 238, primarily due to low sample size of the CPT-II and WCST) and were included in this neuropsychology-referred group. All 76 children completed every memory, verbal and attention/executive tasks. From this total group (NP Group; n ¼ 76), a 1:1 age- and sex-matched control group was obtained from a sample of children who participated in the inpatient program from 2010 to 2015 but did not receive a neuropsychological evaluation (n ¼ 153). This age/sex matching from the sample without a neuropsychological evaluation resulted in a No-NP Group (n ¼ 75). Neuropsychological evaluation within the inpatient program is typically initiated following the initial psychiatric evaluation and conducted over several sessions and/or days depending on the functioning of the child. A standard neuropsychological battery is administered by the clinical neuropsychologist, psychometrician, and/or graduate-level neuropsychology trainee. Age, sex, race, history of legal involvement, use of public insurance, and childhood maltreatment history were used to provide demographic information on the sample. Psychiatric variables included hospitalization length of stay (LOS; in days), status as new admission or re-admission to the hospital, the mean number of diagnoses, rate of diagnostic comorbidity, self-reported anxiety (Multidimensional Anxiety Scale for Children [MASC/MASC-2])/depression (Children’s Depression Inventory [CDI/ CDI-2]) symptoms and the presence of specific psychiatric and neurodevelopmental disorders diagnosed during hospitalization. Mood disorders were categorized into Depressive Disorders (Major Depressive Disorder, Dysthymic Disorder, and Depressive Disorder Not Otherwise Specified), Bipolar Disorder, and (other) Mood Disorders (Mood Disorder Not Otherwise Specified and Disruptive Mood Dysregulation Disorder). Information on medication status at the time of the neuropsychological evaluation was not available; however, medication status at the time of admission was utilized in the present study. The standard practice is for the children to take their medication as usual during their neuropsychological evaluation. Medications at intake were classified into mood stabilizers, anxiolytics, antipsychotics/atypical antipsychotics, anti-depressants (SSRIs and others [e.g., bupropion]), and stimulants/non-stimulants (stimulants [e.g., methylphenidate] and non-stimulants [e.g., guanfacine]). DCYF involvement and maltreatment history were only available for theNP Group. Discharge diagnoses were not available for the No-NP Group (n ¼ 75), while they were available for the NP Group (n ¼ 76). Therefore, No-NP/NP analyses utilized the intake diagnoses, while descriptive data on discharge diagnoses for NP Group are also provided.