Altered attention networks in patients with thyroid dysfunction: A neuropsychological study

Highlights

• Four kinds of thyroid dysfunction existed different characters of ANT performance.

• Impaired attention networks was in patients with hypothyroidism and hyperthyroidism.

• Executive control network was related with T4 in hypothyroidism or hyperthyroidism.

• Emotion had no effect on difference of ANT performance between groups.

• No alterations of attention networks was in subclinical thyroid dysfunction.

Abstract

Patients with thyroid dysfunction (31 hypothyroid, 32 subclinical hypothyroidism, 34 hyperthyroid, and 30 subclinical hyperthyroidism) and 37 euthyroid control subjects were recruited and performed the attention network test (ANT), which can simultaneously examine the alertness, orientation and execution control of the participants. Patients with hypothyroidism had abnormalities in the alerting network, and those with hyperthyroidism had impairments of the alerting and executive control networks. No attention networks deficit existed in patients with subclinical hyperthyroidism and subclinical hypothyroidism. The anxiety and depression scores of patients with thyroid dysfunction were significantly higher than those of the healthy control group. Covariance analysis demonstrated that interactions between group and Hamilton Anxiety Scale scores, group and HAMD score were not significant, but there was a significant main effect for group when analyzing the difference in values of the alerting network between groups. Further, the efficiency of the executive control network was negatively correlated with the T4 level in the hypothyroidism group, and positively correlated with the T4 level in the hyperthyroidism group. T4 or T3 level and efficiencies of the executive control network had a significant quadratic U-shaped relationship in all participants. In summary, the patients with four kinds of thyroid dysfunction exhibited different characteristics of ANT performance. Patients with thyroid dysfunction had various degrees of anxiety and depression disorders, but anxiety and depression disorders had no effect on the differences in the executive control network between the groups.

Introduction

Thyroid dysfunction is a common clinical disease, which includes hypothyroidism, hyperthyroidism, subclinical hypothyroidism, and subclinical hyperthyroidism (M'Rabet-Bensalah et al., 2016; Radhakrishnan et al., 2013; Tasdemir et al., 2015). Laboratory examination of hypothyroidism reveals insufficient levels of serum thyroxine (T4), triiodothyronine (T3) and excessive levels of thyroid stimulating hormone (TSH). The laboratory examination of hyperthyroidism is characterized by increased levels of serum T4 and T3, and decreased levels of serum TSH (Allahabadia et al., 2009; Kravets, 2016). The laboratory examination of subclinical hypothyroidism and subclinical hyperthyroidism reveals abnormally high or low serum TSH levels, combined with serum thyroid hormone (T4, T3) in the normal range, respectively (Biondi et al., 2015; Donangelo and Suh, 2017; Pearce et al., 2013).

A number of pieces of clinical evidence have demonstrated that patients with thyroid dysfunction have some cognitive impairments, including inability to concentrate, forgetfulness, reduced learning ability, and so on (Smith et al., 2015; Vogel et al., 2007). These changes in cognitive function have many adverse effects on patients' quality of life. In 1835, Graves et al. (Graves, 1835) began to report mental and cognitive impairment in patients with thyroid dysfunction. Since then, more studies have been carried out on the effects of thyroid function on cognition (Bavarsad et al., 2019; Dejanovic et al., 2017; Hogervorst et al., 2008; Pasqualetti et al., 2015; Ritchie and Yeap, 2015; Samuels, 2014; Tasdemir et al., 2015; Vogel et al., 2007). Alvarez et al. (Alvarez et al., 1983) used the Tolouse-Pieron Concentration Attention Test to find impaired attention in patients with hyperthyroidism. Constant et al. (Constant et al., 2005) examined the behavior of hypothyroidism patients after thyroidectomy, and the results showed that their attention and executive function were damaged. These findings suggested that patients with thyroid dysfunction manifested a deficit in attentional function, but relatively little is known about the effects of different functional thyroid states on attention networks.

Attention network theory, which is proposed by Posner and Petersen (Petersen and Posner, 2012; Posner and Petersen, 1990), states that attention systems are subdivided into threebrain networks: alerting, orienting, and executive control. The alerting network involves the ability to maintain high sensitivity and phasically responding to incoming information. Previous research has shown that the alerting network is related to some regions of the frontal lobe in the right hemisphere, and the norepinephrine system. The orienting component of attention is defined as the ability to select some items from incoming information by shifting the attentional focus. Neuroimaging and neurobiology evidence has revealed that the orienting network involves the superior and inferior parietal lobe, posterior regions, and the cholinergic system. The executive control network is defined as resolving conflicts between competing information. The dopamine system plays an important part in maintaining the appropriate ability of executive control. According to the attention network theory, Fan and his colleague (Fan et al., 2002) designed the attention network test (ANT), which can measure the alertness, orientation and execution control components of participants at the same time. The test has been used to examine attention networks and distinguish deficits in the various components of attention in many neuropsychiatric diseases (Aboitiz et al., 2014; Pauletti et al., 2017; Yang et al., 2015).

Thyroid hormone and TSH are very important for maintaining normal cognitive function (Accorroni et al., 2017), and they are thought to be related to the synthesis and degradation of neurotransmitters including norepinephrine, dopamine, and choline (Claustre et al., 1996; Mano et al., 1998). These neurotransmitters also play critical roles in regulating the attention networks function. However, the concrete mechanism by which thyroid dysfunction influence attention networks is unclear.

In our study, ANT was used to systematically examine and evaluate the attention function of patients with hypothyroidism, hyperthyroidism, subclinical hypothyroidism and subclinical hyperthyroidism. The aim of our study was to find out whether the attention networks were altered, and the characteristics of impairment in patients with four kinds of thyroid dysfunction.