Diabetes WM qEEG 2019

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NEUCLI 2671 1—11 ARTICLE IN PRESS

Neurophysiologie Clinique/Clinical Neurophysiology (2019) xxx, xxx—xxx
1
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ORIGINAL ARTICLE
2 Type-1 diabetes shapes working memory

3 processing strategies
4 Francisco Javier Alvarado-Rodríguez a, Rebeca Romo-Vázquez b,
5 Geisa Bearitz Gallardo-Moreno a, Hugo Vélez-Pérez b,
6 Andrés Antonio González-Garrido a,∗,1
a
7 Instituto de Neurociencias, CUCBA, Universidad de Guadalajara, 180 Francisco de Quevedo, 44130,
8 Guadalajara, Jalisco, Mexico
b
9 Departamento de Ciencias Computacionales, CUCEI, Universidad de Guadalajara, 1421 Boulevard
10 Marcelino García Barragán, 44430, Guadalajara, Jalisco, Mexico
11 Received 9 June 2019; accepted 30 September 2019
12 KEYWORDS Summary
13 Cognition; Background. — Type 1 diabetes (T1D) is a metabolic disorder characterized by recurrent hypo-
14 EEG; and hyperglycemic episodes, whose clinical development has been associated with cognitive
15 Emotion; and working memory (WM) deficits.
16 qEEG; Objective. — To contrast quantitative electroencephalography (qEEG) measures between young
17 Type 1 diabetes; patients with T1D and healthy controls while performing a visuospatial WM task with two
18 Working memory memory load levels and facial emotional stimuli.
19 Methods. — Four or five neutral or happy faces were sequentially and pseudo-randomly pre-
20 sented in different spatial locations, followed by subsequent sequences displaying the reversed
21 spatial order or any other. Participants were instructed to discriminate between these two
22 alternatives during EEG recording.
23 Results. — A significant increase in the absolute power of the delta and theta bands, distributed
24 mainly over the frontal region was found during task execution, with a slight decrease of alpha
25 band power in both groups but mainly in control individuals. However, these changes were more
26 pronounced in the T1D patients, and reached their maximum level during the WM encoding
27 phase, even on trials with the lower memory load. In contrast, changes seemed to occur more
28 gradually in controls and results differed significantly only on the trials with the higher WM load.
29 Conclusions. — These results reflect adaptive WM-processing mechanisms in which cognitive
30 strategies have evolved in T1D patients in order to meet task demands.
31 © 2019 Elsevier Masson SAS. All rights reserved.
32
∗
Corresponding author at: Instituto de Neurociencias, Universidad de Guadalajara, Francisco de Quevedo 180, Colonia Arcos Vallarta,
Guadalajara, Jalisco, 44130, Mexico.
E-mail address: gonzalezgarrido@gmail.com (A.A. González-Garrido).
1 http://www.ineuro.cucba.udg.mx/.
https://doi.org/10.1016/j.neucli.2019.09.003
0987-7053/© 2019 Elsevier Masson SAS. All rights reserved.
Please cite this article in press as: Alvarado-Rodríguez FJ, et al. Type-1 diabetes shapes working memory processing
NEUCLI 2671 1—11
strategies. Neurophysiologie Clinique/Clinical Neurophysiology (2019), https://doi.org/10.1016/j.neucli.2019.09.003
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2 F.J. Alvarado-Rodríguez et al.
33 Introduction tional adaptive changes as means to maintain cognitive 91
performance, despite the occurrence of glycemic level 92
34 Type 1 diabetes mellitus (T1D) is a disease in which the extremes. Similar to Bolo and colleagues [9], they found no 93
35 beta cells of the pancreatic islets, which produce insulin, statistically-significant differences in the behavioral perfor- 94
36 are attacked and destroyed by the immune system [2]. mance between T1D patients and healthy matched controls 95
37 Insulin plays an important role in metabolizing glucose and, while performing a visuospatial WM task. However, their 96
38 therefore, has an essential function in regulating the energy patients showed greater fMRI activations in the inferior 97
39 supply of the brain, an organ that consumes about 25% of the frontal gyrus, basal ganglia, substantia nigra, and cere- 98
40 glucose available in the body [47]. As a result, T1D is charac- bellum. These subcortical activations, in addition to the 99
41 terized by recurrent hypo- and hyperglycemic episodes that cortical activations usually required for WM processing, 100
42 have a negative impact on the brain. These glycemic fluc- were interpreted as reflecting a compensation mechanism 101
43 tuations have also been related to cognitive deficits that that allowed those patients to maintain a behavioral perfor- 102
44 affect executive functions [23], especially working memory mance similar to that of controls. In accordance with these 103
45 [19,59]. results, and applying the same methodology, but in an effec- 104
46 Executive functions play a pivotal role in goal-directed tive connectivity study, Guàrdia-Olmos and colleagues [28] 105
47 behavior. One core executive function is working memory reported that T1D patients showed a pattern of brain con- 106
48 (WM), which operates by holding information in the mind nectivity distinct from that of healthy controls. In the T1D 107
49 and mentally working with it [4]. WM can be sub-divided group, fewer brain areas were involved in the WM task and 108
50 into several main processing phases: there was a notable lack of involvement of the frontal cor- 109
tical areas, while the red nucleus and cerebellum showed 110
strong connectivity with the core WM network. 111

51 • initial encoding of information; Embury and colleagues [18] also focused on young 112
52 • subsequent maintenance and retrieval of WM items [57]. patients without comorbid conditions and evaluated them 113
while in the normoglycemic range. They argued that this 114
53 Encoding and maintaining visuospatial information in approach would make it possible to reach stronger conclu- 115
54 WM have been associated with increased recruitment sions concerning the unique impact of diabetes on brain 116
55 of attention-associated brain areas, including parietal physiology. Interestingly, they reported no between-group 117
56 and frontal cortices [20,44]. However, when dealing with differences on accuracy rates on a Sternberg-type verbal WM 118
57 different WM load levels, it seems that prefrontal cor- task performed during a magnetoencephalography (MEG) 119
58 tex activity varies depending on the task phase [45]. In study. However, they did find that the T1D patients exhib- 120
59 general, there is agreement on the fact that WM is neces- ited stronger responses in the superior parietal area during 121
60 sary for language comprehension, translating instructions, encoding and diminished alpha response in the parieto- 122
61 incorporating new information into action plans, reason- occipital cortices during the maintenance phase. These 123
62 ing, creativity, and making plans and decisions [16]. Despite authors suggested that this pattern of neural dynamics in 124
63 the growing literature on WM development, its processing their young patients may reflect a compensatory strategy 125
64 mechanisms and primary neurofunctional substrates, the for decreased neural resources or efficiency by using other 126
65 precise mechanisms underlying WM impairments are still network resources, and that this compensation was similar 127
66 poorly understood. to that observed in an aging population. Another key point 128
67 One of the problems linking T1D to WM deficits is that for research in this area consists of examining the differ- 129
68 most of the studies approaching this issue have focused ent phases of WM processing (encoding vs. maintenance) 130
69 on the consequences of glycemic level extremes, often that allows more subtle between-group differences to be 131
70 inducing hypoglycemia to evaluate its effects on control identified. 132
71 participants [1,9,24,59]. As expected, both patients with While fMRI studies have provided valuable information on 133
72 T1D and control individuals are usually affected by induced specific brain pattern differences between patients with T1D 134
73 hypoglycemia in these studies, though the poorer cognitive and healthy controls during WM tasks [9,22], delineating the 135
74 performance of T1D patients is emphasized. In contrast, more active brain areas during each WM processing phase 136
75 Bolo and colleagues [9] failed to find significant differences has been more difficult due to the temporal limitations of 137
76 between patients and controls on accuracy or reaction times this technique. Electroencephalography (EEG), given its high 138
77 while performing a WM task under euglycemic or hypo- accuracy measured in milliseconds, might in contrast reflect 139
78 glycemic conditions. These authors also reported that brain differences in both phases of WM processing; that is, encod- 140
79 regions with a supplementary role in WM function, such as ing and maintenance. Although Embury et al. [18] studied 141
80 the parietal lobe and cerebellum, presented greater fMRI- this issue using MEG in T1D patients, to the best of our knowl- 142
81 BOLD activation in patients during hypoglycemia, suggesting edge, no studies have yet addressed the effects of emotional 143
82 that these areas may have been recruited to help maintain distractors on WM performance in these patients using an 144
83 cognitive performance. electrophysiological approach. 145
84 Other approaches, which did not involve inducing hypo- It is well-known that emotional events influence WM, as 146
85 glycemia, have suggested that young adults with T1D—but occurs in daily life [36,46], and there is compelling evi- 147
86 with average IQ and without comorbidities—already show dence that processes such as attention, decision-making, 148
87 neural processing that is distinct from that of their peers cognitive control, and WM all play central roles in emo- 149
88 without diabetes [18,22]. In this regard, Gallardo-Moreno tion, and that cognition and emotion dynamically influence 150
89 and collaborators [22] argued that the early impact of each other in ways that contribute to adaptive behavior 151
90 this disease during neurodevelopment could lead to func- [17,50]. Understanding the mechanisms underlying these 152
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Type-1 diabetes affects cognitive strategies 3
153 reciprocal interactions is critical for comprehending the fun-

Table 1 Demographic and clinical characteristics of study
154 damentals of healthy functioning. For instance, the stress
participants.
155 caused by glycemic dysregulation, daily insulin injections,
156 a special diet and regular medical checkups in T1D patients Controls T1D patients
157 could interact with cognitive deficits reported in this popula-
158 tion, particularly those affecting executive functions, which n 18 18
159 potentially play a key role in self-management and treat- Age (years) 21.61 (3.94) 22.22 (4.08)
160 ment adherence [11]. Sex (men/women) 11/7 11/7
161 Recently, our group explored WM processing in T1D Education (years) 12.17 (2.43) 11.53 (2.47)
162 patients while manipulating emotional stimuli through fMRI IQ 111.80 (7.41) 106.06 (10.04)
163 methods, using a 2-back task detecting facial identity in HbA1c (%) — 8.64 (1.72)
164 neutral, happy or fearful faces [25]. Significant differences Last fasting plasma — 132.72(48.42)
165 were found between the neurofunctional activation pat- glucose
166 terns of T1D patients and healthy controls, particularly Plasma glucose 87.83 (9.31) 237.11 (106.45)
167 characterized by greater prefrontal activation in patients (before EEG
168 when processing emotional faces, while controls exhibited recording)
169 more activation in parietal regions. The observed group Data are means (standard deviations). n: number of cases;
170 differences were interpreted as the result of a specific inter- HbA1c : glycated hemoglobin.
171 ference effect of the emotional content of the stimuli on
172 WM’s cognitive control in the patient group. Such inter- intention of maximizing their attractiveness, in the context 215
173 ference could elicit attention allocation difficulties and of two different WM load levels. Based on previous studies, 216
174 decrease the operational efficiency of WM. In the light of we hypothesize that the encoding stage of WM processing 217
175 these findings, two additional issues should be further clari- in T1D patients will be more susceptible to the impact of 218
176 fied in this clinical population: the effect of varying levels of highly attention-appealing stimuli, particularly when WM 219
177 working memory load, and the sensitivity of distinct stages load increases. 220
178 of WM processing in the time domain. With the above mentioned purpose, we set out to 221
179 Jin and colleagues [36] found significant effects of evaluate the effect of WM load and two highly attentional- 222
180 emotional content on WM task performance and ERP distracting stimuli on qEEG measures while T1D patients 223
181 correlates with encoding, maintenance and retrieval pro- and controls performed visuospatial WM tasks (distinguishing 224
182 cesses. Specifically, they reported that positive emotions encoding and maintenance/retrieval phases), and compare 225
183 improved WM performance by facilitating maintenance and those results to a task-preceding resting period. 226
184 retrieval processing, while negative content exhibited an
185 enhancement effect only during encoding and maintenance.
186 Guimond and colleagues [29], meanwhile, examined how Methods 227
187 happy and fearful emotional distractors impact performance

188 on WM tasks by varying the cognitive load using the fMRI Participants 228
189 technique. They found that patients with schizophrenia had

190 greater difficulty in performing a WM task than healthy Individuals diagnosed with T1D were recruited from two 229
191 controls when regulating emotions, and suggested that the associations that specialize in treating diabetes mellitus: 230
192 increase in WM load may have placed a high demand on sub- the Endocrinology Services of the Centro Médico Nacional 231
193 jects’ executive networks and interfered with their ability de Occidente and the Fray Antonio Alcalde Hospital. The 232
194 to regulate emotional distractors. These findings led us to sample consisted of 18 T1D patients with at least 8 years 233
195 hypothesize that this could also occur in patients with T1D. of disease evolution who reported adequate adherence 234
196 We agree with Embury and colleagues’ hypothesis [18] that to treatment and optimal daily glucose control, and 18 235
197 the compensatory strategies observed in aging are likely to healthy control individuals matched according to gender, 236
198 also be found in T1D patients. Moreover, Hou and colleagues age and educational level. All participants were right- 237
199 [32] recorded EEGs from healthy adults (young and seniors) handed. Their age range was 14—26 years, and they had 238
200 under three different conditions: resting state, 0-back task, completed at least 9 years of schooling. The T1D patients 239
201 and 2-back task. They found that age-related disturbances (11 males) had a mean age of 21.61 (± 3.94) years (mean 240
202 were more prominent during the high-load task, especially schooling: 11.53 ± 2.47 years), while the matched controls 241
203 in the theta band, and suggested that this band plays an had a mean age of 22.22 (± 4.08) years (mean schooling: 242
204 integrative role on WM tasks that could be attributed to com- 12.17 ± 2.43 years). Table 1 shows the demographic charac- 243
205 pensatory activation in aging. Therefore, it seems that the teristics of the study participants. 244
206 study of different memory loads could reflect subtle differ- All participants had an average IQ (90—110; Wechsler 245
207 ences in brain dynamics between T1D patients and healthy Adult Intelligence Scale: WAIS-IV), and had no antecedents 246
208 participants. In our view, the approach used by Guimond of neurodevelopmental, neurological or psychiatric dis- 247
209 and colleagues [29] and Hou and colleagues [32] to explore orders. According to medical records, the T1D patients 248
210 WM disturbances in this population merits further evalua- had no hospital admissions due to diabetes in the 2 years 249
211 tion. Accordingly, the main aim of the present study was prior to study participation, nor any diabetic complications 250
212 to comparatively explore quantitative EEG measures during (retinopathy, nephropathy or neuropathy). Informed written 251
213 performance of a visuospatial WM task in T1D patients and consent was obtained from participants or their parents, in 252
214 controls, using neutral and happy faces as stimuli, with the the case of minors. The experimental protocol was approved 253
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Figure 1 Example of a sequence with a correct reversed order in the spatial location of the stimuli presentation. Each stimulus
lasted 1000 ms on the screen with variable inter-stimulus intervals and a response time of 1500 ms.
254 by the Ethics Committee of the Neuroscience Institute • resting EEG, which corresponded to a resting period pre- 295
255 (ET112016-226; Universidad de Guadalajara). ceding the task during which subjects simply watched a 296
fixation point displayed in the center of a black back- 297
ground for three minutes; 298
256 Experimental task • visuospatial WM encoding, that is, EEG epochs beginning 299
at the instant when the final stimulus of the first series 300
257 Participants performed a visuospatial working memory task was presented (fourth in the shorter series, fifth in the 301
258 with simultaneous EEG recording. Stimulus delivery and longer ones); 302
259 response collection were controlled by E-prime Studio 2.0 • visuospatial WM maintenance, that is, EEG epochs starting 303
260 software. During experimental sessions, which were always at the instant when the final stimulus of the second series 304
261 scheduled in the morning after having a regular breakfast, was presented (fourth in the shorter series, fifth in the 305
262 participants were seated comfortably in a quiet, dimly-lit longer ones). 306
263 room, 60 cm away from a LCD monitor. They were instructed

264 to focus their attention on a fixation point located in the For practical purposes, from now on we will refer to these 307
265 center of the screen in order to minimize head movements. phases as ‘‘visuospatial encoding’’ and ‘‘visuospatial main- 308
266 The experimental task used neutral (N) and happy (H) faces tenance’’. All EEG epochs selected during these two phases 309
267 as stimuli, which were presented sequentially and pseudo- corresponded only to trials with correct responses and the 310
268 randomly at eight different screen locations. After a short baseline was corrected using each subject’s resting state 311
269 delay of 1000 ms, a second sequence was presented, and average. 312
270 subjects were instructed to press the left button of the
271 mouse if the latter sequence corresponded to the correct
272 inversed spatial order of the first one, but the right but- Artifact rejection 313
273 ton if it did not. Fig. 1 shows the experimental flow chart.
274 The experiment consisted of a total of 120 trials divided into
In order to achieve the maximum number of artifact-free 314
275 three blocks of 40 sequences each, including 60 trials with
EEG epochs per condition, the blind source separation (BSS) 315
276 four stimuli and the other 60 with five, both counterbal-
technique was employed to remove artifacts, which were 316
277 anced across the blocks. Each stimulus lasted 1000 ms with
mainly ocular, according to the methodology presented in 317
278 an inter-stimuli interval of 1000 ms. The presentation order
Romo-Vazquez and colleagues [56]. 318
279 of the blocks was pseudo-randomized.
First, any trial with EOG voltage deflection greater than 319
280 Recognition of the emotional content of the faces used
50 ␮V (relative to baseline) was discarded. Then, an expert 320
281 in this task was previously validated in a group of university
reviewed each EEG recording rejecting the epochs with 321
282 students with the same age range as the participants.
artifacts by visual inspection. Subsequently, EEG segments 322
(20 seconds in length) containing the recordings of interest 323
at the center of the epoch were used for further artifact 324
283 Electrophysiological recordings rejection. Only the source corresponding to the ocular arti- 325
fact was eliminated. Once it was removed, the entire record 326
284 EEGs were recorded from 21 scalp electrodes placed in was rebuilt. Only 11.75% of the data had to be transformed 327
285 accordance with the International 10—20 system (Fp1, Fp2, using the BSS-SOBIRO algorithm [5] due to the presence 328
286 F7, F3, Fz, F4, F8, T3, C3, Cz, C4, T4, T5, P3, Pz, P4, T6, of ocular artifacts. In addition, 2% of the total EEG chan- 329
287 O1, O2) and two periocular electrodes (EOG), all referenced nels were lost, so they were removed from the analysis 330
288 to linked earlobes. A 32-channel electroencephalograph and replaced by the average information for the group 331
289 (MEDICID-04 system) with low and high cut filters set at 0.3 involved. Although similar studies have replaced the infor- 332
290 and 30 Hz, respectively, was used. Interelectrode impedance mation from lost channels with their contralateral measures 333
291 was kept below 5 k . EEG data were digitized at a sampling from the same patient [10,34][e.g. 10,34], we did not 334
292 rate of 200 Hz. employ this method because our aim was to analyze EEG 335
293 Artifact-free, 1000-ms EEG epochs were selected by changes associated with cognitive performance, so replac- 336
294 visual inspection in three different main conditions: ing the information on one side with the data recorded in 337
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Table 2 Behavioral results while performing the experimental task.
Lower WM load Higher WM load

Happy Neutral Happy Neutral
Correct responses (%) Patients 80.74 (13.9) 81.85 (14.9) 80.37 (13.4) 76.30 (15.0)
Controls 89.26 (10.6) 91.67 (7.2) 87.96 (8.8) 82.41 (12.4)
Response times (ms) Patients 541.62 (76.7) 535.52 (86.8) 556.53 (80.9) 550.05 (114.2)
Controls 466.63 (131.3) 458.36 (130.1) 489.25 (137.0) 470.02 (124.2)
Data are means (standard deviations).
338 its contralateral homologous side could have affected the absolute energy of the frequency bands—␦ (1—3 Hz), ␪ 378
339 interpretation of results. (4—7 Hz), ␣ (8—13 Hz) and ␤ (14—30 Hz)—was estimated at 379
each one of the 19 electrode sites. To reduce individual 380
data variability, we analyzed the median of the energy for 381

340 Data analysis
each frequency band by condition (i.e. resting, visuospa- 382
tial encoding, visuospatial maintenance, and two WM load 383

341 All analyses were primarily designed to comparatively eval-
levels), in each subject. 384
342 uate two key effects in T1D patients and healthy controls,
For topographic purposes, and due to the important 385
343 as follows:
role attributed to the frontal (particularly prefrontal) brain 386
region when processing information in WM, EEG power spec- 387

344 • the impact of task performance on quantitative EEG meas- tral measures were evaluated in two main extensive regions: 388
345 ures (absolute power in different frequency bands: delta, frontal (Fp1, Fp2, F3, F4, F7, F8 and Fz), and posterior 389
346 theta, alpha and beta); (O1, O2, P3, P4, Pz, T5 and T6). First, resting qEEG meas- 390
347 • the impact of memory load while using complex emotional ures were analyzed using a Repeated Measure ANOVA with 391
348 facial stimuli [shorter versus longer sequences; i.e. lower Frequency Band (4 levels: delta, theta, alpha, beta) and 392
349 (LL) versus higher (HL) memory load trials]. Group (2 levels: T1D, Controls) as factors. Subsequently, RM- 393
ANOVAs were executed to analyze qEEG while performing 394

350 The analysis of the particular effects of the emotional the task using three within-subject factors: Frequency Band 395
351 content of the stimuli lies beyond the scope of the present (delta, theta, alpha, beta), Task Phase (Encoding, Mainte- 396
352 study; nonetheless their potential impact on behavioral per- nance), and WM load (lower: LL, higher: HL), along with 397
353 formance was properly tested. Group (T1D, Controls) as the between-subject factor. All 398
354 Due to the comprehensive differences in the blood glu- calculations were performed considering an alpha value of 399
355 cose levels between T1D patients and controls prior to the 0.05. Greenhouse-Geisser corrections to the df were applied 400
356 EEG recording, Pearson correlation analyses were performed as needed, with the corrected probabilities reported. Addi- 401
357 with the purpose of exploring this effect on qEEG measures tionally, post hoc tests were calculated to explore any trends 402
358 in both groups. in the observed changes using Bonferroni adjustments for 403
multiple comparisons. 404
359 Behavioral analysis

Results 405
360 Behavioral responses were computed for both groups and
361 analyzed using SPSS (IBM Corp., 2016 release). Analysis of
362 variance (ANOVA) was performed using Group (2: patients, Behavioral results 406
363 controls) as the between-group factor, with WM load (2: LL:

364 shorter sequences; HL: longer sequences) and Emotion [2: The T1D patients achieved a significantly lower number 407
365 (H: trials with happy faces), (N: trials with neutral faces)] of correct responses than controls (F(1,34) = 4.67; P = 0.038) 408
366 as the within-subject factors, along with the percentage of with prolonged reaction times in all conditions (F(1,34) = 4.47; 409
367 correct responses and response times as dependent varia- P = 0.042). The complete behavioral results are summarized 410
368 bles. in Table 2. In addition, WM load influenced the number of 411
correct responses, as participants had a significantly lower 412
number of correct responses during the trials with the higher 413
369 Quantitative EEGs WM load (F(1,34) = 13.52; P = 0.001). In fact, higher WM load 414
level did not affect the number of correct responses when 415
370 Thirty EEG artifact-free epochs corresponding to correct trials with happy facial expressions were evaluated. The 416
371 responses were selected from each subject and condition, statistics on the behavioral results are shown in Table 3. 417
372 while balancing their distribution into three identical blocks
373 of the experimental stream of stimuli (40 sequences each)
374 to avoid confounding effects like initial behavioral adjust- Electrophysiological results 418
375 ments, the settlement of cognitive strategies, fatigue, etc.

376 For each EEG epoch selected, the power spectrum was Quantitative resting phase EEG measures for anterior and 419
377 calculated using Fast Fourier Transformation (FFT). The posterior brain regions failed to show significant differ- 420
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Table 3 Summary results of the ANOVA for behavioral results.
F df P 2 1-ˇ
Correct responses Load 13.520 1,34 0.001 0.285 0.946

Emotion 3.420 1,34 0.073 0.091 0.435
Group 4.667 1,34 0.038 0.121 0.555
Load*Group 1.066 1,34 0.309 0.030 0.171
Emotion*Group 0.003 1,34 0.956 0.000 0.050
Load*Emotion 8.673 1,34 0.006 0.203 0.816
Load*Emotion*Group 0.387 1,34 0.538 0.011 0.093
Response Times Load 3.816 1,34 0.059 0.101 0.475
Emotion 1.839 1,34 0.184 0.051 0.261
Group 4.466 1,34 0.042 0.116 0.537
Load*Group 0.022 1,34 0.883 0.001 0.052
Emotion*Group 0.255 1,34 0.617 0.007 0.078
Load*Emotion 0.250 1,34 0.621 0.007 0.077
Load*Emotion*Group 0.218 1,34 0.643 0.006 0.074
F: Snedecor’s F statistic; P: statistical significance; df: degrees of freedom; 2 : effect size; 1-ˇ: statistical power.
421 ences between the groups in both the overall power and was significantly lower in controls. Figs. 2 and 3 show 438
422 in the individual frequency bands. Even though we did the spatial representation of the absolute power for 439
423 not observe significant behavioral results for the emotional delta and theta frequency bands, respectively. Besides, 440
424 facial stimuli, we decided to analyze its possible influence the significant interaction between Frequency Band and 441
425 on qEEG. However, no significant effects were found. We Task Phase (F(3,102) = 4.07, P = 0.009, 2 = 0.107, 1-ˇ = 0.832) 442
426 did observe that the spectral power measurements tended showed a relevant decrease of beta power from encoding 443
427 to be lower in T1D than controls, but this tendency reversed to maintenance in WM. An additional relevant interac- 444
428 during task performing periods, thus probably contributing tion between Frequency Band and WM load (F(3,102) = 29.06, 445
429 to the final outcomes. P < 0.001, 2 = 0.461, 1-ˇ = 1.00) revealed that delta, theta, 446
430 While performing the task, the results for the anterior and beta powers significantly increased during higher 447
431 brain region revealed significant effects for the factors Fre- WM load trials, with delta showing the highest incre- 448
432 quency Band (F(3,102) = 24.56, P < 0.001, 2 = 0.419, 1-ˇ = 1.00) ment (P < 0.001). The significant interaction between Task 449
433 and WM load (F(1,34) = 15.69, P < 0.001, 2 = 0.316, 1-ˇ = Phase and WM load (F(1,34) = 17.48, p < 0.001, 2 = 0.340, 1- 450
434 0.97). There was a significant interaction between Fre- ˇ = 0.982) denoted that main changes between Task Phases 451
435 quency Band and Group (F(3,102) = 4.39, P = 0.006, 2 = 0.114, occurred during LL (P < 0.001), even though there were also 452
436 1-ˇ = 0.861), indicating that delta and theta powers were significant changes during HL (P = 0.04). Finally, a signifi- 453
437 significantly higher in T1D patients, while alpha power cant interaction was found between Frequency Band, Task 454
Figure 2 Spatial representation of the absolute power of the delta band—normalized with respect to the energy measured during
resting in the same group—in the two main experimental visuospatial WM phases and WM load levels, for both T1D patients and
controls.
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Figure 3 Spatial representation of the absolute power of the theta band—normalized with respect to the energy measured during
controls.
455 Phase and WM load (F(3,102) = 14.81, P < 0.001, 2 = 0.303, 1- Task Phase (F(3,102) = 47.71, P < 0.001, 2 = 0.584, 1-ˇ = 1.00), 466
456 ˇ = 1.00), reinforcing the notion that delta and theta powers exposing the significant increase of delta power during the 467
457 significantly varied during LL in both Task Phases (P < 0.001, visuospatial WM maintenance (see Fig. 1). Another signif- 468
458 and P = 0.04, respectively), while significant variations on icant interaction between Frequency Band and WM load 469
459 alpha and beta powers were restricted to HL (P = 0.011, and (F(3,102) = 16.54, P < 0.001, 2 = 0.327, 1-ˇ = 1.00) described 470
460 P = 0.003, respectively). how HL condition determined a relevant increment for 471
461 On the other hand, statistical analysis of the posterior delta power and a slight decrement in alpha power. Fig. 4 472
462 region showed significant effects for Frequency Band depicts the spatial distribution of the absolute power of the 473
463 (F(3,102) = 34.31, P < 0.001, 2 = 0.502, 1-ˇ = 1.00) and Task alpha frequency band. Ultimately, the interaction between 474
464 Phase (F(1,34) = 25.43, p < 0.001, 2 = 0.428, 1-ˇ = 0.998), Task Phase and WM load (F(1,34) = 4.21, P = 0.04, 2 = 0.110, 475
465 with significant interactions between Frequency Band and 1-ˇ = 0.513) showed that greater changes between the 476
Figure 4 Spatial representation of the absolute power of the alpha band—normalized with respect to the energy measured during
controls.
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477 WM load levels occurred during the encoding phase, while even though this emotional content is not relevant to task 534
478 greater changes between Task Phases occurred during LL completion. 535
479 trials. Second, although there is at yet no general consensus on 536
this topic, the role of delta waves during mental tasks has 537
480 Correlation analyses been associated with cortical deafferentation or the inhibi- 538
tion of the sensory afferences that interfere with internal 539
concentration [30,31]. In fact, interference control is con- 540

481 Correlation analyses between blood glucose levels and EEG
sidered an executive-attention function of the prefrontal 541
482 quantitative measures failed to show significant effects.
cortex [21] in which attention is expedited by suppressing 542
483 However, delta power at frontal regions, during both encod-
distraction; thus, the presence of EEG delta oscillations may 543
484 ing (r = 0.465, P = 0.05) and maintenance (r = 0.441, P = 0.06)
signal the inhibition of other processes that could interfere 544
485 stages, reached an achievable tendency exclusively in
with solving the mental task (see [30], for a comprehensive 545
486 healthy individuals while processing the lower level WM
review]. In the present experiment, patients showed signif- 546
487 load.
icant frontal increase of delta energy during encoding that 547
was only seen in controls on the trials with the higher WM 548
488 Discussion load. This result reinforces the notion that even lower WM 549
load levels might demand more processing resources in T1D 550
489 The main aim of the present work was to characterize elec- patients. Moreover, these additional efforts seem to per- 551
490 trophysiologically the dynamic brain activity of young people sist over frontal areas in patients during WM maintenance, 552
491 with T1D and healthy controls during WM encoding and main- also involving posterior locations, as observed in the control 553
492 tenance associated with the execution of a cognitive task, group. 554
493 while evaluating the effect of the WM load level using faces Furthermore, our T1D patients showed a substantial 555
494 as stimuli. This was done by adding a differential emotional increase of the absolute power of the theta band in frontal 556
495 content, irrelevant to task fulfilment, in order to enhance areas during the WM encoding phase, which was only seen 557
496 attentional distraction. in controls while performing the higher WM load level. 558
497 Although neuropsychological evaluation did not discern Increased frontal theta activity has been shown to corre- 559
498 signs of cognitive impairment, the behavioral results for the late positively with visual working memory capacity [38], 560
499 experimental task showed significant between-group dif- increased WM load [49], and coding of new information [41]. 561
500 ferences, as the T1D patients showed a lower number of This suggests that frontal theta activity is associated with 562
501 correct responses with prolonged reaction times. Though enhanced motivation and attention [38]. Recently, it has 563
502 not statistically significant, similar behavioural trends been proposed that during stimulus encoding, the theta fre- 564
503 have been observed in T1D patients with good glycemic quency band produces a positive subsequent memory effect 565
504 control [22,27]. and that the magnitude of frontal post-encoding-related 566
505 Despite the observed behavioral differences, an impor- theta activity correlates with the discrimination accuracy 567
506 tant and necessary distinction between the clinical of the test stimulus [55]. Moreover, recent evidence sug- 568
507 characteristics of the current group of T1D patients and gests that oscillations in frontal theta power reflect specific 569
508 those regularly reported in the literature must be made. control adjustments of behavior [14]; thus, they are consid- 570
509 This is because all our experimental subjects had regu- ered a neural marker of mid-prefrontal cortex engagement 571
510 lar medical follow-ups and no hospital admissions due to to support goal-directed control [12,13]. All these find- 572
511 diabetes in the 2 years prior to their participation in this ings suggest that the differences observed in the absolute 573
512 study. Also, they had a higher mean educational level than theta power in our groups could also reinforce the idea 574
513 that corresponding to the Mexican population as a whole, that they represent part of the additional cognitive efforts 575
514 coupled with optimal daily glucose control. In this con- required by T1D patients to fulfill task demands. In addi- 576
515 text, differences in cognitive processing between the groups tion, they support previous hypotheses assuming that T1D 577
516 may be interpreted as being caused directly by the impact patients need to deploy greater processing resources in 578
517 of the illness on central nervous system development and order to match the cognitive processing level shown by 579
518 current operation. controls [9,22]. 580
519 Behavioral responses showed two clear additional find- No significant differences were found between T1D 581
520 ings in both groups. First, an increase in WM load generated patients and controls for the absolute powers of delta and 582
521 a significant reduction in the number of correct responses, theta bands during resting. In contrast, slight decreases 583
522 though this effect was not seen when happy faces were in delta and theta activity were previously described at 584
523 used as stimuli. This finding is consistent with previ- rest for T1D patients without antecedents of early severe 585
524 ous reports which postulate that emotional information hypoglycemia [3]. Several other studies, however, have 586
525 can enhance and facilitate episodic memory consolidation reported an increase in the energy of the slower fre- 587
526 [43,48], WM capacity [51], n-back task performance [15], quency bands in patients with diabetes during rest, but 588
527 and visuospatial WM abilities [26]; thus facilitating WM this has been attributed mainly to a history of severe 589
528 processing on more difficult trials probably via greater cor- hypoglycemia [7,8,10,33] or to the hypoglycemic state 590
529 tex activation associated with what has been defined as itself [54,60,61]. 591
530 ‘‘emotional attention’’ [52,53]. Stated briefly, under cer- Another relevant result, which is worth pointing out, is 592
531 tain circumstances—such as in the present experiment—the that controls showed widespread significantly lower alpha 593
532 emotional nature of stimuli can attract additional atten- activity while performing the task with respect to T1D 594
533 tional processing resources and so facilitate task execution, patients. This difference may be related to an effect on 595
NEUCLI 2671 1—11
+Model
596 the implementation of inhibitory processes [35,58] that has Despite limitations due primarily to the relatively small 654
597 been associated with the alpha band [6,42]. In fact, alpha sample size, this study found specific interactions between 655
598 band frequencies have been largely associated with spatial WM load and task performance in a context in which the 656
599 attention [37,40] even though their actual functional role is stimuli presented were emotional faces, and was able to 657
600 still under debate. Recently, Keitel and colleagues [39] pos- discern, electrophysiologically, between T1D patients and 658
601 tulated that the attentional modulation of dynamic visual healthy controls during the different steps of WM processing. 659
602 stimulation relies on cortical mechanisms, including retino- These findings suggest the need to continue analyzing these 660
603 topic alpha suppression. In this context, the dissimilarity effects using other types of cognitive tasks, and to evaluate 661
604 between T1D and controls on task-related alpha band activ- the potential specific contributions of other variables, such 662
605 ity might imply that T1D patients fail to dynamically control as sex, age, and years of disease evolution, among others. 663
606 their spatial attention, at least with similar efficiency to

607 controls.
608 One remarkable point was the lack of significant correla- Funding 664
609 tion between the blood glucose level at the beginning of the
610 experiment and qEEG measures. This result emphasizes the This work was supported by SEP-PRODEP NTPC Mexico, 665
611 notion that spectral parameters of the EEG are relatively project number 12967810-245213-511-6/18-9169/UDG-PTC- 666
612 stable, thus increasing its usefulness to study pathologi- 1413, 2018. 667
613 cal conditions. In this regard, the tendency observed in

614 healthy individuals to relate glycemia and delta power could
615 represent a physiological adaptive response to preserve
Disclosure of interest 668
616 homeostasis; such a mechanism would be probably affected

617 by the progress of a metabolic disease as T1D. The authors declare that they have no competing interest. 669
618 Taken together, the effects found on quantitative EEG

619 measures from the earlier steps of WM processing (encod-
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2 Type-1 diabetes shapes working memory

11 Received 9 June 2019; accepted 30 September 2019

33 Introduction tional adaptive changes as means to maintain cognitive 91

performance, despite the occurrence of glycemic level 92

strong connectivity with the core WM network. 111

while in the normoglycemic range. They argued that this 114

70 inducing hypoglycemia to evaluate its effects on control identiﬁed. 132

83 cognitive performance. electrophysiological approach. 145

153 reciprocal interactions is critical for comprehending the fun-

187 happy and fearful emotional distractors impact performance

189 technique. They found that patients with schizophrenia had

ﬁxation point displayed in the center of a black back- 297

ground for three minutes; 298

263 room, 60 cm away from a LCD monitor. They were instructed

(20 seconds in length) containing the recordings of interest 323

Table 2 Behavioral results while performing the experimental task.

Lower WM load Higher WM load

each one of the 19 electrode sites. To reduce individual 380

data variability, we analyzed the median of the energy for 381

tial encoding, visuospatial maintenance, and two WM load 383

region when processing information in WM, EEG power spec- 387

ANOVAs were executed to analyze qEEG while performing 394

multiple comparisons. 404

359 Behavioral analysis

363 controls) as the between-group factor, with WM load (2: LL:

368 bles. in Table 2. In addition, WM load inﬂuenced the number of 411

correct responses, as participants had a signiﬁcantly lower 412

375 ments, the settlement of cognitive strategies, fatigue, etc.

Table 3 Summary results of the ANOVA for behavioral results.

Correct responses Load 13.520 1,34 0.001 0.285 0.946

479 trials. Second, although there is at yet no general consensus on 536

tion of the sensory afferences that interfere with internal 539

concentration [30,31]. In fact, interference control is con- 540

load levels might demand more processing resources in T1D 550

518 current operation. controls [9,22]. 580

606 their spatial attention, at least with similar efﬁciency to

613 cal conditions. In this regard, the tendency observed in

616 homeostasis; such a mechanism would be probably affected

618 Taken together, the effects found on quantitative EEG

630 failure in the ‘‘on-line’’ evaluation of cognitive demands, 2011;54:2404—8. 680

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