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Background: Attention ability can be subdivided into three functionally independent networks, i.e., alerting net‑ work, orienting network, and executive network. Previous literature has documented that deficits in attention are a common consequence of HIV infection. However, the precise nature of deficits of attention in HIV ‑ infected patients is poorly understood. Accordingly, the aim of the study was to identify whether the HIV‑ infected patients showed a specific attention network deficit or a general attentional impairment. Methods: We investigated 27 HIV‑ infected patients and 31 normal controls with the Attention Network Test (ANT ). Results: The patients exhibited less efficient alerting network and executive network than controls. No significant difference was found in orienting network effect between groups. Our results also indicate a tendency for poorer efficiency on alerting attention and executive attention in patients with CD4 ≤ 200. Conclusions: Our findings suggest that HIV ‑ infected patients exhibited selective impairments of attention network of alerting and executive control. The link between lower CD4 T cell count and poorer attention network function imply the importance of starting antiretroviral therapy earlier to avoid irreversible neurocognitive impairment. Keywords: HIV, Attention network test, Alerting, Orienting, Executive episodic memory, and etc. . Additionally, neuroim- Background aging studies have found HIV-infected patients exhib- HIV-associated neurocognitive disorders (HAND) are ited hyperactivity in task-related brain regions despite characterized by disabling cognitive, behavioral and equal performances as controls [9, 10], suggesting that motor dysfunction , and are a common hallmark of functional compensation by increasing usage of neural HIV infected individuals. Although the introduction of reserves to maintain cognitive performance. combination antiretroviral treatment (cART) has sig- Attention is a core property in human information pro- nificantly reduced the prevalence of more severe form of cessing , which enables us to process behaviorally rel- HAND [2, 3], the incidence of less severe forms of HAND evant information for the guidance of our responses . (i.e., asymptomatic neurocognitive impairment and mild For HIV-infected patients, deficits in attention are a com - neurocognitive disorder) remain common among HIV mon consequence of HIV infection [13, 14] and the one patients in the cART era [3–5]. Given the predominance of the neurocognitive domains affected early in progres - of the milder forms of HAND [4, 6, 7], considerable sion of HIV [14, 15]. Although attention plays the central researches have been conducted to elucidate the compo- role in patients’ driving ability  and was associated with nent processes of HAND across the domains of informa- poor medical adherence , the precise nature of deficits tion processing speed, executive functions, motor skills, in attention for HIV-infected patients is poorly understood . In previous studies of HAND, attentional functioning *Correspondence: firstname.lastname@example.org was routinely investigated by clinical neuropsychological Department of Brain Functioning Research, The Seventh Hospital of Hangzhou, 305 Tianmushan Road, Hangzhou 310013, Zhejiang, China tests. While the neuropsychological approach has its clinical Full list of author information is available at the end of the article © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Wang et al. Behav Brain Funct (2017) 13:11 Page 2 of 9 convenience, it also has two main disadvantages. Firstly, testing clinic at Hangzhou Center for Disease Control although these studies considered attention as one of a and Prevention. Among these patients, there were thir- number of distinguishable cognitive domains, the neuropsy- teen patients were diagnosed with AIDS, according to chological tests using in these researches required multiple the clinical history of AIDS defining illnesses or the nadir cognitive abilities for successful performance . Secondly, CD4 T cell count below 200 cells per microliter. In addi- this approach pertained merely to matters of overall atten- tion, there were twenty patients with nadir CD4 T cell tional functioning rather than the structures of attention. count below 400 per microliter, including twelve patients The lack of consistency in the definition of attention  being treated with highly active antiretroviral therapies would make it difficult to compare results across studies. (HAART) containing a HIV protease inhibitor and eight Conceptually, attention is not a single entity, but is patients that refused HAART therapy. comprised of multiple components. According to the The average nadir CD4 T cell count for all patients was attention network theory, this basic and sophisticated 298.41 (SD = 223.58) cells per microliter. According to cognitive ability can be subdivided into three functionally the previous literature , to study the possible associa- independent networks, i.e., alerting network, orienting tion between a nadir CD4 T cell count and the pattern network, and executive network [18, 19]. In this frame, of attention network function, all patients were divided the alerting network allows maintenance of a vigilant into patients with CD4 ≤ 200 (n = 12) and patients with and alert state, the orienting network allows for select- CD4 > 200 (n = 15). ing the information through the space, and the executive Thirty-one healthy controls with no HIV-infection his - network is responsible for solving the conflict between tory were recruited from local community to serve as a expectation, stimulus, and response . control group. All participants were interviewed by an The Attention Network Test (ANT) was developed to experienced clinical psychologist with the Structured assess the ability of these three separate networks. The Clinical Interview for DSM-IV (SCID)  and met the efficiency of each network is calculated by averaging following inclusion criteria: (a) negative family history reaction times across several different cue and flanker of any psychiatric disorders, (b) no evidence of current conditions. Since the initial description of the ANT , or previous head injury, CNS disease or DSM-IV Axis I attention network function has been examined using the disorder, (c) no evidence of current alcohol or substance ANT in different clinical population, including schizo - abuse, and (d) no evidence for severe opportunistic infec- phrenia , depression , ADHD , 22q11 dele- tions. All participants were over 18 years of age and tion syndrome , multiple sclerosis , and etc. These right-handed, with normal vision and hearing. Written studies suggested that most of these neuropsychiatric and informed consent was obtained from all participants. populations exhibited a specific attention network deficit The details of participants were shown in Table 1. rather than a general attention deficit. As described above, although deficits in attention are ANT deemed as the one of cognitive declines among HIV- The details of ANT  are illustrated in Fig. 1. At the infected patients, however, previous studies failed to beginning of each trial, a fixation cross was presented in address whether the HIV-infected patients showed a the center of the screen for a random variable duration specific attention network deficit or a general attentional (400–1600 ms). Then, a warning cue was presented for impairment. Accordingly, we examined HIV-infected 100 ms. After a short fixation period (400 ms), the target patients with the attention network test, to better under- appeared and participants were required to determine stand the nature of attentional deficits in the population. whether a central arrow point left or right. Participants were required to focus on centrally located fixation cross Methods throughout the task, and to response by pressing the key- Participants and procedures board direction key as fast and accurately as possible. A total of twenty-seven patients with HIV-1 infection There are four different cue conditions: (1) no cue, par - were recruited through the voluntary counseling and ticipants were shown a fixation cross which was the same Table 1 Comparisons of demographic between groups (mean ± SD) Normal controls (n = 31) HIV-infected patients (n = 27) Statistics Sex ratio (M: F) 18:13 17:10 χ = 0.145, p = 0.704 Index age (years) 30.97 ± 12.83 (16–60) 32.26 ± 7.31 (21–45) F = 0.213, p = 0.646 Education levels (years) 11.81 ± 4.42 (4–17) 10.48 ± 4.64 (4–18) F = 1.241, p = 0.270 Wang et al. Behav Brain Funct (2017) 13:11 Page 3 of 9 Fig. 1 The diagram of attention network test as the first fixation across; (2) center cue, in which an each condition. Relative to no cue condition, double cues asterisk was presented at the central fixation across; (3) tend to alert the participants to the imminent appearance double cue, in which an asterisk was presented on above of the target in the two potential target locations. Accord- and below the fixation cross, separately and simultane - ingly, the alerting effect was calculated by subtracting the ously; (4) spatial cue, in which an asterisk was presented mean of medians under the double cue condition from on the target location (either above or below the central the mean under medians of the no cue condition. Both fixation point). Also, there are three target conditions: (1) spatial cues and central cues provide alerting information neutral target, there was only one central arrow; (2) con- for the imminent appearance of the target, but only the gruent target, the target (i.e., central arrow) was flanked spatial cues provide predictive spatial information about on either side by two arrows in the same direction; (3) the appropriate location begin the target arrives. Thus, the incongruent target, the target was flanked on either side orienting effect was calculated by subtracting the mean of by two arrows in the opposite direction. medians under the spatial cue condition from the mean Each trial lasted for 4000 ms. In total, there were one of medians under the center cue condition. Regarding tar- practice block and three experimental blocks. The prac - get conditions, participants had to overcome the conflict tice block consisted of 24 trials with feedback on their elicited by the distracting flankers in the incongruent con - speed and accuracy. Each experimental block consisted dition, whereas they did not in congruent condition. The of 96 trials without feedback. executive effect was calculated by subtracting the mean of medians under the congruent condition from the mean of Calculation of attention network efficiencies medians under the incongruent condition. The manipulations of cue and target allow the calculation of response time (RT) difference assumed to represent the Statistics three attention networks. According to previous litera- Pearson’s Chi squared test was carried out to assess the ture [21, 28], to avoid the influence of the outliers, wrong sex ratio between groups. Multivariate analysis of vari- responses, RT outside a 100–1700 ms window and RT ance (MANOVA) was performed for index age and edu- outside two standard deviations of each condition were cational level between HIV-infected patients and normal excluded step by step. Then, medians were calculated for controls. Wang et al. Behav Brain Funct (2017) 13:11 Page 4 of 9 To provide a comprehensive description of the controls, but approximately equal RT with normal con- results, we first conducted a three-way repeated analy - trols in no cue condition and spatial cue condition. sis of variance (repeated measures ANOVA) with groups (HIV-infected patients vs. normal controls) as a between- Repeated measures ANOVA for accuracy subjects factor and cue conditions (no cue, center cue, Repeated measures ANOVA results showed a significant double cue, and spatial cue), and target conditions (neu- main effect of target conditions (i.e., participants made tral, congruent, and incongruent) as within-subject fac- more errors in incongruent condition than others) [F tors, and with response time and accuracy as dependent (2112) = 10.876, P < 0.001]. The interaction between cue variables. To clarify which conditions are driving the conditions and target conditions approached significance difference of three attentional network effects between [F (6336) = 2.225, P = 0.040]. As Fig. 2c shows, the effect HIV-infected patients and normal controls, we con- of cue conditions was enhanced when given incongru- ducted repeated measures ANOVAs with the medians of ent target than that in others. No other significant main response time as dependent variables to explored main effects and interactions were found for accuracy. effects of alerting cue conditions (i.e., double cue vs. no cue), orienting cue conditions (i.e., spatial cue vs. center Repeated measures ANOVA for medians of response time cue), and executive target conditions (i.e., incongru- between normal controls and HIV-infected patients ent target vs. congruent target), and its interaction with Repeated measures ANOVA for medians of response groups. time showed significant main effects of alerting cue Finally, to explore the possible association between a conditions (i.e., longer medians in no cue than double nadir CD4 T cell count and the pattern of attention net- cue) [F (156) = 146.386, P < 0.001], orienting cue con- work function, MANOVA with post hoc test by Bonfer- ditions (i.e., longer medians in center cue than spatial roni was conducted for three attentional network effects, cue) [F (156) = 102.671, P < 0.001], and executive target mean RT, and overall accuracy among groups (i.e., conditions (i.e., longer medians in incongruent target patients with CD4 ≤ 200, patients with CD4 > 200, and than congruent target) [F (156) = 102.671, P < 0.001] [F normal controls). (156) = 430.346, P < 0.001]. There was a significant interaction between alerting Results cue conditions and groups [F (156) = 11.948, P = 0.001]. Demographic data As Fig. 3a shows, participants in group of HIV-infected Table 1 summarizes the demographic characteristics showed longer medians in double cue condition than between the patients and controls. Analyses of Variance normal controls, but approximately equal medians with and Chi Squared tests revealed no significant differences normal controls in no cue condition. No significant inter - in index age, education levels, and sex ratio. action was found between orienting cue conditions and groups [F (156) = 0.143, P = 0.707]. As Fig. 3b shows, Repeated measures ANOVA for RT both HIV-infected patients and normal controls showed Table 2 summarized the performance in ANT for each longer medians in center cue condition than spatial cue group. Repeated measures ANOVA results showed a sig- condition. Repeated measures ANOVA also indicated a nificant main effect of cue conditions (i.e., longer RT in significant interaction between executive target condi - no cue condition than others, and shorter RT in spatial tions and groups [F (156) = 5.800, P = 0.019]. As Fig. 3c condition than others) [F (3168) = 131.757, P < 0.001]. shows, participants in group of HIV-infected showed There was significant main effect of target conditions (i.e., longer medians in incongruent target condition than longer RT in incongruent than others and shorter RT in normal controls, but approximately equal medians with neutral) [F (2112) = 447.633, P < 0.001]. No significant normal controls in congruent target condition. main effect of group was found for RT [F (156) = 0.016, P = 0.899]. Attentional network effects among groups There was a significant interaction between cue condi - Table 3 summarized three attentional network effects tions and target conditions [F (6336) = 5.848, P < 0.001]. for each group. MANOVA results showed that there As Fig. 2a shows, the effect of the target conditions was was a significant main effect of groups on alerting effect enhanced when given double cues and center cues than [F (255) = 7.261, P = 0.002] and executive effect [F that in no cue condition and spatial cue condition. Addi- (255) = 3.208, P = 0.048], but not on orienting effect [F tionally, there was a significant interaction between cue (255) = 1.348, P = 0.268]. No significant differences were conditions and group [F (3168) = 3.362, P = 0.020]. As found between groups for mean RT [F (255) = 1.236, Fig. 2b shows, participants in group of HIV-infected P = 0.298] and overall accuracy [F (255) = 0.761, showed longer RT in double cue condition than normal P = 0.472]. Wang et al. Behav Brain Funct (2017) 13:11 Page 5 of 9 ‑ ‑ Table 2 Mean RT and accuracy under each condition for each group No cue Double cue Center cue Spatial cue Mean Normal HIV-infected Normal HIV-infected Normal HIV-infected Normal HIV-infected Normal HIV-infected controls patients controls patients controls patients controls patients controls patients Mean RT and standard deviations Congruent 709 (123) 695 (99) 653 (104) 668 (83) 673 (100) 668 (94) 640 (105) 630 (93) 669 (108) 666 (95) Incongru 792 (121) 802 (85) 768 (110) 782 (83) 773 (104) 791 (83) 723 (106) 747 (88) 764 (110) 781 (85) ent Neutral 634 (118) 619 (101) 574 (89) 585 (85) 586 (101) 596 (87) 569 (93) 570 (88) 591 (100) 593 (90) Mean 712 (121) 706 (95) 665 (101) 678 (87) 677 (101) 685 (88) 644 (101) 649 (89) 674 (106) 679 (90) Accuracy and standard deviations Congruent 0.98 (0.07) 0.99 (0.04) 0.97 (0.07) 1.00 (0.02) 0.98 (0.07) 0.99 (0.06) 0.98 (0.07) 0.99 (0.03) 0.98 (0.07) 0.99 (0.04) Incongru 0.96 (0.08) 0.98 (0.04) 0.95 (0.08) 0.98 (0.05) 0.94 (0.09) 0.97 (0.06) 0.95 (0.08) 0.98 (0.06) 0.95 (0.08) 0.98 (0.05) ent Neutral 0.97 (0.08) 0.98 (0.08) 0.97 (0.07) 0.98 (0.03) 0.98 (0.07) 0.98 (0.05) 0.97 (0.08) 0.98 (0.05) 0.97 (0.07) 0.98 (0.06) Mean 0.97 (0.07) 0.98 (0.06) 0.97 (0.07) 0.99 (0.04) 0.96 (0.08) 0.98 (0.05) 0.97 (0.08) 0.98 (0.05) 0.97 (0.08) 0.98 (0.05) Wang et al. Behav Brain Funct (2017) 13:11 Page 6 of 9 Fig. 3 The diagram of the interactions between different conditions for medians of RT Post-hoc tests by Bonferroni showed that the patients with CD4 ≤ 200 exhibited less efficient alerting atten - tion than normal controls (P = 0.002). The difference between the patients with CD4 ≤ 200 and normal con- trols approached significance (P = 0.062). No other sig- nificances were found between-groups comparisons (all P ≥ 0.347). Discussion Fig. 2 The diagram of the significant interactions between differ ‑ Attention is the core cognitive ability to select some ent conditions for RT. No significant interaction between target aspects of the world and ignore others for further pro- conditions and group was found [F (2112) = 1.442, P = 0.241]. No significant interaction between cue conditions, target conditions and cessing [11, 29]. While this basic ability enables the acqui- group was found [F χ(6336) = 1.645, P = 0.134] sition of skills in other cognitive areas, few studies in Wang et al. Behav Brain Funct (2017) 13:11 Page 7 of 9 Table 3 Comparisons of ANT performance between groups (Mean ± SE) Normal controls HIV-infected patients (n = 27) Statistics (n = 31) CD4 > 200 (n = 12) CD4 ≤ 200 (n = 15) Overall Alerting effect (ms) 47.06 ± 3.73 32.27 ± 5.88 18.58 ± 6.58 26.19 ± 4.90 F = 7.261, p = 0.002 Orienting effect (ms) 31.35 ± 4.02 40.40 ± 6.25 25.42 ± 6.99 33.74 ± 5.16 F = 1.348, p = 0.268 Executive effect (ms) 92.84 ± 4.92 111.60 ± 9.99 124.17 ± 11.17 117.19 ± 9.32 F = 3.208, p = 0.048 Mean RT (ms) 669.19 ± 31.97 636.87 ± 37.35 724.42 ± 41.75 675.78 ± 18.90 F = 1.236, p = 0.298 Overall accuracy (%) 96.16 ± 1.23 97.33 ± 1.53 98.58 ± 1.71 97.89 ± 4.49 F = 0.761, p = 0.472 HIV-infected adults have employed measures specifically values were significantly lower in HIV-infected sub - designed to assess different components of attentional jects than HIV-seronegative group [35, 36]. In addition, ability. For its advantage of allowing for comparison of Kumar et al. reported a strong correlation between spe- the relative deficits in different attention network , cific HIV-1 viral load increases and dopamine reduction the attention network test (ANT) has been widely used in within the Substantia Nigra . different neuropsychological population. In the present Unlike the findings of alerting attention and execu - work, we first adopted ANT to test whether the HIV- tive attention, our results indicate that HIV-infected infected patients showed a specific attention network patients were equally sensitive to the spatial cues with deficit or a general attentional impairment. normal controls. These seem to suggest that the orient - Our results show that HIV-infected patients exhibited ing attention function was intact in these patients. The longer medians in double cue condition than normal intact orienting attention function found in HIV-infected controls, whereas made approximately equal medians patients is not unique. Using ANT, we have also found with normal controls in no cue condition. This result that an intact orienting attentional ability in patients indicate that HIV-infected patients showed less advan- with depression , untreated hyperthyroidism , tage from a warning cue for preparation for detecting and the breast cancer patients receiving chemotherapy an expected signal, and suggest that they exhibited less treatment . Previous studies have documented that efficient alerting attention function. This finding is con - cholinergic systems arising in the basal forebrain appear sistent with the neurotransmitter hypothesis underlying to play a critical role in orienting attention network [18, alerting attention. It is believed that the alerting attention 41, 42]. Further research should be conducted to exam- is related to norepinephrine function . Patients with ine whether this cholinergic systems are not vulnerable to HIV-infection often complained about their difficulty in HIV infection. maintaining a vigilant state [15, 30]. And, previous stud- Consistent with previous literature [43–46], our results ies have reported that the norepinephrine response to a also indicate a tendency for poorer efficiency on alert - cold pressor test  and the sympathetic activity  in ing attention and executive attention in patients with HIV-infected subjects was blunted. Our result also indi- CD4 ≤ 200. Although this finding was limited by small cate HIV-infected patients showed longer medians in sample size, the link between lower CD4 T cell count incongruent target condition than normal controls, while and poorer attention network function has revealed the made approximately equal medians with normal controls importance of the CD4 nadir as a marker of neurocogni- in congruent target condition. These findings suggest that tive deficits. As Muñoz-Moreno et al.  proposed, neu - patients with HIV-infection exhibited less efficient exec - rocognitive functioning is likely to be more affected when utive attention function, and had difficulty in resolving more systemic immunosuppression appears. In addition, response conflicts between competing information. This a recent study has documented those reductions in brain is consistent with previous neuropsychological studies volumes in HIV-infected patients are strongly linked in HIV-infection. Deficits in executive domain of atten - to a history of immunosuppression with lower nadir tion control have been reported in previous studies using CD4 count . This finding, combined with other evi - the trail making test , and the Stroop task . Also, dences, suggests that it would be wiser to start antiretro- this is in agreement with the neurotransmitter hypothesis viral therapy earlier to avoid irreversible neurocognitive underlying executive attention. It is demonstrated that impairment. the dopamine function plays a prominent role in execu- Some limitations with regard to the present study tive attention network . And, previous studies have should be mentioned. For absence of day-to-day func- reported that the cerebrospinal fluid dopamine mean tioning scores in HIV-infected patients, it is not known Wang et al. Behav Brain Funct (2017) 13:11 Page 8 of 9 Funding whether there is an association between everyday func- This work was supported by the National Natural Science Foundation of China tioning and the three attention network effects. The lack (Grant No. 81471366), the Science and Technology Bureau of HangZhou of clinically-relevant information about HIV disease (Grant No. 20150733Q33), the Science and Technology Bureau of HangZhou (Grant No. 20170533B51), and the Science and Technology Bureau of Wen‑ prognosis also makes it difficult to interpret these find - Zhou (2015Y0410). ings within the context of HIV disease. Finally, our sam- ple size was small, which increases the risk of type II Publisher’s Note error. In sum, although limited by a small sample size, Springer Nature remains neutral with regard to jurisdictional claims in pub‑ our findings suggest that HIV-infected patients exhibited lished maps and institutional affiliations. selective impairments of attention network of alerting Received: 14 February 2017 Accepted: 30 May 2017 and executive control. It would be wiser to start antiret- roviral therapy earlier to avoid irreversible neurocogni- tive impairment. Conclusions References 1. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, et al. The use of ANT allowed us to address whether the atten - Updated research nosology for HIV‑associated neurocognitive disorders. tional deficits in HIV-infected patients was a specific Neurology. 2007;69:1789–99. attention network deficit or a general attention deficit. 2. Brew BJ. AIDS dementia complex. In: Brew BJ, editor. HIV neurology. Oxford: Oxford University Press; 2001. p. 276. 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Behavioral and Brain Functions – Springer Journals
Published: Jun 27, 2017
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