Wu SX, Liang XL, Zhu QQ, Wang W, Jiang L, Chen HH, Tian S, Qi M. Altered hippocampal subfield volumes are associated with memory and executive function in patients with type 2 diabetes mellitus. World J Diabetes 2025; 16(7): 104424 [DOI: 10.4239/wjd.v16.i7.104424]
Corresponding Author of This Article
Ming Qi, MD, Associate Professor, Chief Physician, Department of Radiology, The First Affiliated Hospital with Nanjing Medical University, No. 300 Guangzhou Road, Gulou District, Nanjing 210029, Jiangsu Province, China. qiming@njmu.edu.cn
Research Domain of This Article
Radiology, Nuclear Medicine & Medical Imaging
Article-Type of This Article
Case Control Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Shu-Xian Wu, Qin-Qin Zhu, Li Jiang, Shui Tian, Ming Qi, Department of Radiology, The First Affiliated Hospital with Nanjing Medical University, Nanjing 210029, Jiangsu Province, China
Xiao-Long Liang, Huan-Huan Chen, Department of Endocrinology, The First Affiliated Hospital with Nanjing Medical University, Nanjing 210029, Jiangsu Province, China
Wei Wang, Department of Radiology, Liyang People's Hospital, Changzhou 213300, Jiangsu Province, China
Co-first authors: Shu-Xian Wu and Xiao-Long Liang.
Co-corresponding authors: Shui Tian and Ming Qi.
Author contributions: Wu SX and Liang XL contribute equally to this study as co-first authors; Tian S and Qi M contribute equally to this study as co-corresponding authors; Qi M, Chen HH and Tian S conceived and designed this study; Wu SX, Liang XL, Zhu QQ, Wang W, Jiang L performed the research; Wu SX, Liang XL analyzed the data; Wu SX, Tian S wrote the paper; all authors reviewed and gave final approval of submission.
Supported by the Bethune Charitable Foundation, No. Z04JKM2022E035; and the Liyang City's 2023 Annual research and development Plan Follows Nanjing Project, No. LC2024001.
Institutional review board statement: This study was abided by the ethical guidelines of the World Medical Association Declaration of Helsinki and was approved by the Local Medical Ethics Committee of the first Affiliated Hospital of Nanjing Medical University.
Informed consent statement: All participants provided written informed consent and were compensated financially for their participation.
Conflict-of-interest statement: All authors report no conflicts of interests.
STROBE statement: The authors have read the STROBE Statement—checklist of items, and the manuscript was prepared and revised according to the STROBE Statement—checklist of items.
Data sharing statement: The codes and dataset are available from the corresponding author upon reasonable request.
Open Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Ming Qi, MD, Associate Professor, Chief Physician, Department of Radiology, The First Affiliated Hospital with Nanjing Medical University, No. 300 Guangzhou Road, Gulou District, Nanjing 210029, Jiangsu Province, China. qiming@njmu.edu.cn
Received: December 28, 2024 Revised: March 17, 2025 Accepted: June 10, 2025 Published online: July 15, 2025 Processing time: 198 Days and 23.2 Hours
Abstract
BACKGROUND
Increasing evidence has shown that hippocampal damage serves as a marker of early cognitive decline in patients with type 2 diabetes mellitus (T2DM); however, the association between hippocampal subregion volume changes and cognitive decline in different dimensions remains unclear.
AIM
To investigate changes in hippocampal subregion volumes in patients with T2DM and their relationship with cognitive function impairment.
METHODS
Sixty patients with T2DM and 32 healthy controls were recruited. All participants underwent a 3.0 T magnetic resonance scan and a series of clinical assessments. Hippocampal subfield volumes were determined using FreeSurfer 7.4.1. A two-sample t-test was used to evaluate group differences. Partial correlation analysis was performed to assess the relationship between hippocampal subregion volumes and cognitive function. aP < 0.05 was considered statistically significant.
RESULTS
Compared with controls, the volume of right hippocampus-amygdala transition area (t = -3.053, P = 0.003) in patients with T2DM was significantly reduced, which was negatively correlated with the required time of the Trail Making Test (TMT)-A (r = -0.331, P = 0.028) and TMT-B (r = -0.402, P = 0.007) and positively correlated with the scores of Symbol Digit Modalities Test (r = 0.381, P = 0.011), Auditory Verbal Learning Test (AVLT)-N7 (r = 0.309, P = 0.041), and Digital Span Test (r = 0.300, P = 0.048). The volume of the right molecular layer (t = -2.998, P = 0.004) was also significantly reduced, which was positively associated with the scores of AVLT-N7 (r = 0.311, P = 0.045). In addition, the left hippocampal fissure volume (t = 3.617, P = 0.002) was significantly increased in patients with T2DM.
CONCLUSION
Declines in cognitive performance, especially memory and executive function, are linked to changes in the volumes of the right hippocampus-amygdala transition area and right molecular layer in patients with T2DM.
Core Tip: This study examines changes in hippocampal subregion volumes in patients with type 2 diabetes mellitus (T2DM) and their relationship with cognitive function impairment. It was found that declines in memory and executive function in patients with T2DM were related to changes in hippocampal subregion volumes, indicating that the hippocampus could serve as a marker for the early diagnosis of cognitive decline in patients with T2DM.
Citation: Wu SX, Liang XL, Zhu QQ, Wang W, Jiang L, Chen HH, Tian S, Qi M. Altered hippocampal subfield volumes are associated with memory and executive function in patients with type 2 diabetes mellitus. World J Diabetes 2025; 16(7): 104424
Over the past three decades, the prevalence of diabetes has increased globally. The most recent data issued by the International Diabetes Federation indicate that the global population of adults with diabetes in 2015 was 415 million and is anticipated to reach 783.2 million by 2045[1]. Disorders in blood glucose stabilization not only affect the kidneys, eyes, and peripheral nervous system but are also associated with cognitive impairments[2]. Diabetes and its associated complications can induce short-term and permanent cognitive abnormalities[3]. Patients with type 2 diabetes mellitus (T2DM) may exhibit modest cognitive impairment, particularly with regard to executive function, delayed memory, and information processing speed[4], which can lead to a decline in their quality of life, lower their sense of wellbeing, and cause considerable inconvenience to patients with T2DM. Compared to people without diabetes, the risk of cognitive impairment and severe depression in patients with diabetes is increased by 1.25-1.91 times and 1.73 times, respectively[5,6]. Therefore, it is crucial to identify biomarkers of cognitive decline in patients with T2DM and intervene in disease progression to prevent or delay cognitive impairment.
Patients with T2DM experience brain atrophy and cerebrovascular disease. Compared with non-diabetic patients, those with diabetes have significantly reduced brain volume in local areas, including the frontal and occipital lobes, deep gray matter, and hippocampus[7]. Compared with other brain regions, the hippocampus is more susceptible to the influence of blood glucose levels owing to the abundance of glucose receptors in the hippocampus[8]. Chronic hyperglycemia is toxic to microvascular endothelial cells and causes oxidative stress through increased advanced glycation end products, lipid peroxidation, and an imbalance in the production of reactive oxygen species and their scavengers[9], thereby leading to neuronal dysfunction and apoptosis. In addition, cerebral vascular lesions caused by chronic hyperglycemia can reduce cerebral blood flow, resulting in ischemia and hypoxia in the hippocampus, ultimately leading to neuronal cell apoptosis and a decrease in hippocampal volume. Inflammatory factors can exacerbate the impact on the structure and function of the hippocampus through oxidative stress reactions[10,11]. Insulin and insulin-like growth factors can play important regulatory roles in neural stem cell self-renewal and neurogenesis through different ligand interactions. Insulin resistance may weaken hippocampal neurogenesis. The decline in overall cognitive function in patients with T2DM is related to changes in hippocampal volume[12], and the reduction in the volume of the left hippocampus-amygdala transition area is significantly correlated with the chronic course of depression[13]. More importantly, the hippocampus is likely to be the initial area impacted by T2DM; thus, damage to the hippocampus could serve as a marker for the early diagnosis of cognitive decline in patients with T2DM[14].
However, the hippocampus has a heterogeneous structure and comprises multiple types of neurons[15]. Different subregions have different functions. Each subregion participates in and collaborates with the others and are deeply involved in memory and cognitive activities[16,17]. With regard to functional distinction, atrophy of the Cornu Ammonis (CA)1 and CA4 regions is associated with a decline in verbal memory and free recall abilities, while a reduction in the volume of the dentate gyrus may affects the formation of new memories[18]. Atrophy of the hippocampus is related to cognitive impairment in various diseases, such as depression, autism spectrum disorder, and Alzheimer's disease[19-21]. However, most studies have examined the hippocampus as a whole, and few have examined the internal structural changes in hippocampal atrophy. The relation between volume changes in these hippocampal subregions and cognitive decline is still unclear, especially in memory and executive function.
Thus, we aim to explore whether there is hippocampal subregion volume atrophy in patients with T2DM, and its relationship with cognitive impairment. We propose that patients with T2DM have atrophy in hippocampal subregions, and this atrophy in distinct hippocampal subregions is involved in cognitive decline in patients with T2DM, such as memory and executive function.
MATERIALS AND METHODS
Participants
From January 2022 to May 2024, 60 patients with type 2 diabetes and 32 healthy controls (HCs) were recruited from the Department of Endocrinology at the First Affiliated Hospital of Nanjing Medical University. The two groups were matched based on sex, age, and years of education. The diagnosis of type 2 diabetes complied with the American Diabetes Association standards[22], and all participants were right-handed, aged between 26 and 76 years, and had more than 6 years of formal education.
The exclusion criteria were as follows: (1) Patients with endocrine system problems, such as hyperthyroidism and hypercortisolism; (2) Those with cerebral hemorrhage, cerebral infarction, brain tumor, and other brain diseases; (3) Patients with other mental and nervous system diseases affecting cognitive function; (4) Pregnant or lactating women; (5) Those having recurrent episodes of hypoglycemia on the test day; (6) Patients who had taken medications that may influence cognitive brain function, such as sertraline, citicoline, and benzodiazepines; and (7) Those with magnetic resonance imaging (MRI) scanning contraindications, such as claustrophobia and metal implants. All the participants provided written informed consent. This study was approved by the Ethics Committee of the First Affiliated Hospital of Nanjing Medical University.
Assessment of cognitive function
A series of clinical scales were used to evaluate each participant’s cognitive function and mental condition. The Montreal Cognitive Assessment and Mini-Mental State Examination tested total cognitive function, with values ranging from zero to 30, where high levels indicate better cognitive function[23]. The Hamilton Anxiety Rating Scale and Hamilton Depression Rating Scale were used to assess the patients' mental states, including anxiety, depression, and other emotions. High scores reflect a more substantial degree of severity. Memory function was evaluated using an Auditory Verbal Learning Test (AVLT), Digital Span Test (DST), and a memory scale. The DST scale required participants to recite numbers forward or backward and was used to evaluate the number of digits remembered. The AVLT assessed the ability to recall words at various times following each trial, indicating immediate recollection, short-delayed recall, and long-delayed memory. Higher scores reflect stronger memory function[24]. The Trail Making Test (TMT) was divided into two parts: A and B. The longer it takes to finish the scale, the lower the executive function. The Symbol Digit Modalities Test (SDMT) assessed participants’ ability to flip between a sequence of numbers and symbols to measure their attention and processing speeds.
MRI acquisition
MRI data were obtained using a Siemens 3.0T magnetic resonance scanner and a 24-channel head coil. T1-weighted magnetic resonance images were obtained using 3D-Magnetization Prepared Rapid Gradient Echo sequences. The scanning parameters were as follows: Repetition time = 1900 ms, echo time = 2.45 ms, flip angle = 9°; field of view = 256 mm × 256 mm; matrix size = 256 × 256; voxel size = 1 mm × 1 mm × 1 mm; slice thickness = 1 mm; slice distance = 0 mm; and volume = 176. Fluid-attenuated inversion recovery sequences were used to rule out organic brain diseases.
Data processing
We used Freesurfer 7.4.1 software to separate the bilateral hippocampi (http://surfer.nmr.mgh.harvard.edu). First, we completed the pre-processing procedures (the ‘recon-all’ command), which included head motion correction, standardized processing of diverse signal intensities, nonlinear registration, the removal of irrelevant regions, such as the head and neck, and cortical segmentation. The hippocampus was automatically segmented based on a manually partitioned map of ultrahigh-resolution MRI images[25]. The hippocampus was divided into 12 subregions: The hippocampal tail, subiculum, CA1, presubiculum, molecular layer, granular cell-molecular layer-dentate gyrus, CA3, CA4, hippocampal fissure, parasubiculum, fimbria, and hippocampal amygdala transition area (HATA; Figure 1). Furthermore, we obtained the estimated total intracranial volume (eTIV) and utilized it as a covariate in the follow-up statistics.
Figure 1 Hippocampal subregion volumes with significant group differences and their correlations with cognitive scales.
A: Significant differences in hippocampal subregion volumes between type 2 diabetes mellitus (T2DM) and healthy control groups; B and C: Hippocampal subregions in a coronal view of a patient with T2DM; D-H: Partial correlation coefficient of cognitive function with the right Hippocampus amygdala transition area volume in patients with T2DM; I: Partial correlation coefficient of cognitive function with the right molecular layer volume in patients with T2DM. aP < 0.05, bP < 0.01. T2DM: Type 2 diabetes mellitus; HC: Healthy control; TMT: Trail Making Test; DST: Digital Span Test; SDMT: Symbol Digit Modalities Test; AVLT: Auditory Verbal Learning Test; CA: Cornu ammonis; GC: Granular cell; DG: Dentate gyrus; HATA: Hippocampus amygdala transition area.
Statistical analysis
SPSS Statistics 25 was used for the demographic, clinical, and image data analyses. The χ2 test was used to compare categorical data, which were reported as percentages. For quantitative data, the mean ± SD was used for expression, and the two-sample t-test was used to evaluate group differences. A P value of < 0.05 was considered statistically significant.
Partial correlation analysis was performed to assess the relation between hippocampal subregion volumes and cognitive functions in patients with T2DM, with sex, age, education level, and eTIV as covariates. The results were corrected for multiple comparisons using the false discovery rate method (aP < 0.05).
RESULTS
General characteristics and cognitive assessments
Owing to the large amplitude of head movements, we included 55 patients with T2DM and 30 HC. There were no significant differences between the two groups regarding sex or body mass index. Patients in the T2DM group were slightly older than those in the HC group (t = 2.144; P = 0.035). The T2DM group had lower DST, SDMT, AVLT-N7, and AVLT-total scores than those in the HC group. There were no significant differences in Hamilton Anxiety Rating Scale and Hamilton Depression Rating Scale scores between the two groups. Demographics, clinical characteristics, and cognitive assessments are presented in Table 1. As hypertension, hyperlipidemia, smoking, drinking, a family history of diabetes, depression, anxiety, and obesity may affect cognitive function in patients with T2DM[26,27], we compared the cognitive function of patients with and without these risk factors. It was found that patients with T2DM who also had hypertension, hyperlipidemia, a history of smoking, depression, anxiety, and obesity exhibited more severe cognitive impairment (Supplementary material).
Table 1 Demographic, clinical, and neuropsychological characteristics of the participants.
After controlling for sex, age, years of education, and diabetes course, bilateral hippocampal volumes were not significantly different between patients with T2DM and HCs. However, compared with the HC group, the volume of the right hippocampal tail (t = -3.501; P = 0.001; Cohen's d = 0.903), right CA1 (t = -2.92; P = 0.005; Cohen's d = 0.752), right molecular layer (t = -2.998; P = 0.004; Cohen's d = 0.755), and right HATA (t = -3.053; P = 0.003; Cohen's d = 0.765) in patients with T2DM were significantly reduced, whereas the volume of the left hippocampal fissure (t = 3.617; P = 0.002; Cohen's d = 0.808) was significantly increased (Table 2).
Table 2 Between‐group differences in hippocampal subfield volume (mm3).
The partial correlation results are shown in Figure 1. The reduction in the right HATA volume in patients with T2DM was negatively correlated with the time required for the TMT-A (r = -0.331; P = 0.028) and TMT-B (r = -0.402; P = 0.007). The reduction in right HATA volume also positively correlated with memory function, as reflected by the scores of AVLT-N7 (r = 0.309; P = 0.041) and DST (r = 0.300; P = 0.048). In addition, the reduction in right HATA volume in patients with T2DM was positively correlated with SDMT scores (r = 0.381; P = 0.011).
The volume decrease in the right molecular layer in patients with T2DM was positively associated with the scores of AVLT-N7 (r = 0.311; P = 0.045), with sex, age, education level, and eTIV as covariates.
DISCUSSION
This study explored the volume changes in hippocampal subregions in patients with T2DM and their relation to memory and executive function. Patients with T2DM have cognitive decline, especially in memory and executive function, which is more prevalent and significant[3,28,29] than impairments in olfactory and visual abilities[30-32] and slower information processing[33]. We found that the DST, SDMT, AVLT-N7, and AVLT total scores in the T2DM group were lower than those in the HC group, which is consistent with the results of previous studies. Furthermore, patients with risk factors, such as hypertension, hyperlipidemia, a history of smoking, depression, anxiety and obesity, experienced more severe cognitive function deterioration. Studies have indicated that hyperglycemia, hypertension, and hyperlipidemia often coexist, and their impacts on cognitive function may be cumulative. These risk factors are all closely associated with heightened systemic inflammation and oxidative stress levels, by promoting the release of pro-inflammatory cytokines. These cytokines can traverse the blood-brain barrier to enter the central nervous system, activate microglia, trigger neuroinflammation, and thereby impair cognitive function[34]. Smoking further exacerbates this damage, synergistically enhancing the inflammatory effects of hyperlipidemia and hypertension. In addition, depression and anxiety can damage neuroplasticity, promote neuronal atrophy and reduce the number and function of synapses[19,35], and lead to reduced sleep quality, thereby leading to cognitive function decline[26,27].
Patients with T2DM have abnormalities in hippocampal structure and function[14,36]. The overall bilateral hippocampal volume in patients with T2DM showed a decreasing trend compared with that in the control group. Our main finding was that, compared with the HC group, the volumes of the right hippocampal tail, right CA1, right molecular layer, and right HATA in patients with T2DM were significantly reduced. In the trisynaptic pathway, CA1 is responsible for the output of information processed by the dentate gyrus to other brain regions, such as the deep structures of the thalamus and the entorhinal cortex[37,38]. Additionally, neurons in the hippocampal CA1 region play an important role in recognizing the identities of other people[39]. These neurons help us retrieve relevant information about others from memory and update this information during interactions, which are essential for forming social relationships. Thus, atrophy of CA1 may induce or exacerbate the decline in memory function in patients with T2DM. In addition, the left hippocampal fissure was significantly larger in patients with T2DM than in the control group. The hippocampal fissure is positioned between the dentate gyrus and the subiculum, and enlargement of the hippocampal fissure may represent atrophy of the medial temporal lobe[40-42].
We also analyzed the correlation between volume changes in the hippocampal subregions and cognitive function in patients with T2DM. The results showed that the reduction in the right HATA volume in patients with T2DM was correlated with some cognitive assessment scores, suggesting that the decline in memory and executive function in patients with T2DM was related to the volume change of the right HATA. As a critical component of the hippocampal-amygdala network, the HATA is neuroanatomically and functionally interconnected with both the hippocampus and amygdala, which are components of the limbic system. It is closely related to neural activities, such as emotions, memory, and learning[43-45]. Consequently, a reduction in the HATA volume disrupts the hippocampal-amygdala network and leads to a decline in cognitive ability.
The molecular layer is part of the dentate gyrus and is rich in dendrites of granule cells and perforant path fibers that transmit sensory information from the entorhinal cortex[46]. It plays an important role in memory formation, especially in the processes of pattern separation and pattern completion[47,48]. Our results showed that a reduction in the volume of the right molecular layer positively correlated with the AVLT-N7 score, indicating that molecular layer atrophy was associated with poor memory function. Animal studies have shown that a hyperglycemic state reduces the density of dendritic spines and the activity of hippocampal neurons in rats[49,50]. Our results emphasize the role of hippocampal circuit atrophy, specifically in the HATA and molecular layer regions, in the decline of memory and executive function in these patients. These findings align with previous studies that have identified decreased volumes in the HATA and molecular layer as potential contributors to cognitive impairment in T2DM[12]. However, different to our findings, some studies have reported a significant reduction in the volume of the hippocampal subiculum and presubiculum, and hippocampal tail in patients with T2DM[13,28]. This discrepancy may be due to differences in diabetes duration, glycemic control, and sample size.
Our findings revealed an asymmetry in hippocampal atrophy, with more pronounced atrophy observed in the right hippocampus than in the left, which is consistent with previous studies[51]. This may be due to apoptosis of hippocampal neurons induced by T2DM, with a more significant impact on the right side of the hippocampus[52]. Studies have shown an asymmetry in synaptic plasticity and memory function between the left and right hippocampal hemispheres[53], contributing in a complementary way to spatial memory and navigation[54]. Consequently, the underlying mechanisms contributing to the lateralization of hippocampal atrophy remain unclear. Genetic regulation, age, and environmental stimulation may be factors contributing to the lateralization of hippocampal volume[55]. In this study, patients with T2DM were older than those in the HC group, which may account for the more pronounced lateralized atrophy of the right hippocampus. In future research, we will expand the sample size and focus on a specific age group for investigation.
This study has several limitations. First, the sample size was relatively small, and future research should include a larger sample. Second, this was a cross-sectional study. Longitudinal studies should be conducted in the future to evaluate the effects on hippocampal subregion volumes through imaging and clinical follow-up. Finally, patients with T2DM are prescribed various medications that may exert subtle effects on cognitive function or brain volume, and we will focus on the therapeutic effect of particular drugs in future research. Further investigations are needed to minimize such bias.
CONCLUSION
We demonstrated that the volumes of various hippocampal subregions were reduced in patients with T2DM. Notably, the atrophy observed in the right HATA and right molecular layer correlated with declines in both memory and executive function, thereby providing a theoretical foundation for the early assessment of multidimensional cognitive decline in patients with T2DM. Additionally, clinical studies have shown that metformin can improve cognitive function in patients with T2DM. As the hippocampus is involved in cognitive regulation and linked to endocrine function, our findings may provide a subtle biomarker for tracking for the cognitive-enhancing effect of metformin.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Endocrinology and metabolism
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade A, Grade A, Grade B, Grade B, Grade B, Grade C
Novelty: Grade B, Grade B, Grade B, Grade C
Creativity or Innovation: Grade B, Grade B, Grade B, Grade C
Scientific Significance: Grade A, Grade B, Grade B, Grade B
P-Reviewer: Aktas G; Horowitz R; Rizwan M; Yuan S; Zhang JJ S-Editor: Lin C L-Editor: A P-Editor: Zheng XM
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