Skip to main content
SpringerLink
Log in

Morphological changes in subregions of hippocampus and amygdala in major depressive disorder patients

  • ORIGINAL RESEARCH
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Despite many neuroimaging studies in the past years, the neuroanatomical substrates of major depressive disorder (MDD) subcortical structures are still not well understood. Since hippocampus and amygdala are the two vital subcortical structures that most susceptible to MDD, finding the evidence of morphological changes in their subregions may bring some new insights for MDD research. Combining structural magnetic resonance imaging (MRI) with novel morphometry analysis methods, we recruited 25 MDD patients and 28 healthy controls (HC), and investigated their volume and morphological differences in hippocampus and amygdala. Relative to volumetric method, our methods detected more significant global morphological atrophies (p<0.05). More precisely, subiculum and cornu ammonis (CA) 1 subregions of bilateral hippocampus, lateral (LA) and basolateral ventromedial (BLVM) of left amygdala and LA, BLVM, central (CE), amygdalostriatal transition area (ASTR), anterior cortical (ACO) and anterior amygdaloid area (AAA) of right amygdala were demonstrated prone to atrophy. Correlation analyses between each subject’s surface eigenvalues and Hamilton Depression Scale (HAMD) were then performed. Correlation results showed that atrophy areas in hippocampus and amygdala have slight tendencies of expanding into other subregions with the development of MDD. Finally, we performed group morphometric analysis and drew the atrophy and expansion areas between MDD-Medicated group (only 19 medicated subjects in MDD group were included) and HC group, found some preliminary evidence about subregional morphological resilience of hippocampus and amygdala. These findings revealed new pathophysiologic patterns in the subregions of hippocampus and amygdala, which can help with subsequent smaller-scale MDD research.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abercrombie, H. C., et al. (1998). Metabolic rate in the right amygdala predicts negative affect in depressed patients. Neuroreport, 9, 3301.

    Article  CAS  PubMed  Google Scholar 

  • Adolphs, R., Tranel, D., & Damasio, H. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372, 669–672.

    Article  CAS  PubMed  Google Scholar 

  • Ahmari, S. (2015). Neuroscience: Inside the fear factor. Nature, 524, 34–34.

    Article  CAS  Google Scholar 

  • Airaksinen, E., Wahlin, Å., Forsell, Y., & Larsson, M. (2007). Low episodic memory performance as a premorbid marker of depression: Evidence from a 3-year follow-up. European Psychiatry, 115, S221–S221.

    Article  Google Scholar 

  • Angelucci, F., Brenè, S., & Mathé, A. A. (2005). BDNF in schizophrenia, depression and corresponding animal models. Molecular Psychiatry, 10, 345.

    Article  CAS  PubMed  Google Scholar 

  • Ballmaier, M., et al. (2008). Hippocampal morphology and distinguishing late-onset from early-onset elderly depression. American Journal of Psychiatry, 165, 229–237.

    Article  PubMed  Google Scholar 

  • Bannerman, D. M., Sprengel, R., Sanderson, D. J., Mchugh, S. B., Rawlins, J. N. P., Monyer, H., & Seeburg, P. H. (2014). Hippocampal synaptic plasticity, spatial memory and anxiety. Nature Reviews Neuroscience, 15, 181–192.

    Article  CAS  PubMed  Google Scholar 

  • Bech, P., Allerup, P., Gram, L. F., Reisby, N., Rosenberg, R., Jacobsen, O., & Nagy, A. (1981). The Hamilton Depression Scale. Acta Psychiatrica Scandinavica, 63, 290–299.

    Article  CAS  PubMed  Google Scholar 

  • Brewer, W. F. (1986). Autobiographical Memory International Encyclopedia of the Social & Behavioral. Sciences, 3, 282–288.

    Google Scholar 

  • Bus, B. A. A., Molendijk, M. L., Tendolkar, I., Penninx, B. W. J. H., Prickaerts, J., Elzinga, B. M., & Voshaar, R. C. O. (2015). Chronic depression is associated with a pronounced decrease in serum brain-derived neurotrophic factor over time. Molecular Psychiatry, 20, 602.

    Article  CAS  PubMed  Google Scholar 

  • Cádiz-Moretti, B., Abellán-Álvaro, M., Pardo-Bellver, C., Martínez-García, F., & Lanuza, E. (2017) Afferent and efferent projections of the anterior cortical amygdaloid nucleus in the mouse. Journal of Comparative Neurology, 525, 2929–2954.

  • Carlesimo, G. A., Piras, F., Orfei, M. D., Iorio, M., Caltagirone, C., & Spalletta, G. (2015). Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer's disease. Alzheimers Dement, 1, 24.

    Google Scholar 

  • Caspi, A., et al. (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science, 301, 386–389.

    Article  CAS  PubMed  Google Scholar 

  • Cavedo, E., et al. (2011). Local amygdala structural differences with 3T MRI in patients with Alzheimer disease. Neurology, 76, 727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, M. C., Hamilton, J. P., & Gotlib, I. H. (2010). Decreased hippocampal volume in healthy girls at risk of depression. Archives of General Psychiatry, 67, 270.

    Article  PubMed  PubMed Central  Google Scholar 

  • Christensen, G. E., Rabbitt, R. D., & Miller, M. I. (2002). Deformable templates using large deformation kinematics. IEEE Transactions on Image Processing A Publication of the IEEE Signal Processing. Society, 5, 1435–1447.

    Google Scholar 

  • Chung, M. K., Dalton, K. M., & Davidson, R. J. (2008). Tensor-based cortical surface morphometry via weighted spherical harmonic representation. IEEE Transactions on Medical Imaging, 27, 1143–1151.

    Article  PubMed  Google Scholar 

  • Ciocchi, S., et al. (2010). Encoding of conditioned fear in central amygdala inhibitory circuits. Nature, 468, 277.

    Article  CAS  PubMed  Google Scholar 

  • Cole, J., et al. (2010). Subregional hippocampal deformations in major depressive disorder. Journal of Affective Disorders, 126, 272–277.

    Article  PubMed  PubMed Central  Google Scholar 

  • Collins, D. L., Neelin, P., Peters, T. M., & Evans, A. C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. Journal of Computer Assisted Tomography, 18, 192.

    Article  CAS  PubMed  Google Scholar 

  • Czéh, B., & Lucassen, P. J. (2007). What causes the hippocampal volume decrease in depression? Are neurogenesis, glial changes and apoptosis implicated? European Archives of Psychiatry and Clinical Neuroscience, 257, 250–260.

    Article  PubMed  Google Scholar 

  • Dannlowski, U., et al. (2007). Amygdala reactivity to masked negative faces is associated with automatic judgmental bias in major depression: a 3 T fMRI study. Journal of Psychiatry & Neuroscience Jpn, 32, 423.

    Google Scholar 

  • Davatzikos, C. (1996). Spatial Normalization of 3D Brain Images Using Deformable Models. Journal of Computer Assisted Tomography, 20, 656–665.

    Article  CAS  PubMed  Google Scholar 

  • Dimsdalezucker, H. R., Ritchey, M., Ekstrom, A. D., Yonelinas, A. P., & Ranganath, C. (2018). CA1 and CA3 differentially support spontaneous retrieval of episodic contexts within human hippocampal subfields. Nature Communications, 9, 294.

    Article  CAS  Google Scholar 

  • Dudek, S. M., Alexander, G. M., & Farris, S. (2016). Rediscovering area CA2: unique properties and functions. Nature Reviews Neuroscience, 17, 89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eldridge, L. L., Engel, S. A., Zeineh, M. M., Bookheimer, S. Y., & Knowlton, B. J. (2005). A dissociation of encoding and retrieval processes in the human hippocampus. Journal of Neuroscience the Official Journal of the Society for. Neuroscience, 25, 3280–3286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Etkin, A., Klemenhagen, K. C., Dudman, J. T., Rogan, M. T., Hen, R., Kandel, E. R., & Hirsch, J. (2004). Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron, 44, 1043–1055.

    Article  CAS  PubMed  Google Scholar 

  • Ferrari, A. J., Somerville, A. J., Baxter, A. J., Norman, R., Patten, S. B., Vos, T., & Whiteford, H. A. (2013). Global variation in the prevalence and incidence of major depressive disorder: a systematic review of the epidemiological literature. Psychological Medicine, 43, 471–481.

    Article  CAS  PubMed  Google Scholar 

  • First M, Spitzer R, Gibbon M, Williams J (2002) Structured Clinical Interview for DSM-IV Axis I disorders

  • Fonberg, E. (1981) Manipulation of various aspects on the emotional behavior by amygdalar lesions and imipramine treatment. Brain & Behaviour, 17, 487-494

  • Fossati, P., Harvey, P. O., Bastard, G. L., Ergis, A. M., Jouvent, R., & Allilaire, J. F. (2004). Verbal memory performance of patients with a first depressive episode and patients with unipolar and bipolar recurrent depression. Journal of Psychiatric Research, 38, 137–144.

    Article  PubMed  Google Scholar 

  • Frodl, T., et al. (2002). Enlargement of the amygdala in patients with a first episode of major depression. Biological Psychiatry, 51, 708.

    Article  PubMed  Google Scholar 

  • Frodl, T., et al. (2003). Larger amygdala volumes in first depressive episode as compared to recurrent major depression and healthy control subjects. Biological Psychiatry, 53, 338.

    Article  PubMed  Google Scholar 

  • Golomb, J., Leon, M. J. D., Kluger, A., George, A. E., Tarshish, C., & Ferris, S. H. (1993). Hippocampal Atrophy in Normal Aging: An Association With Recent Memory Impairment. Archives of Neurology, 50, 967–973.

    Article  CAS  PubMed  Google Scholar 

  • Gould, N. F., et al. (2007). Performance on a virtual reality spatial memory navigation task in depressed patients. American Journal of Psychiatry, 164, 516–519.

    Article  PubMed  Google Scholar 

  • Greenberg, P. E., & Birnbaum, H. G. (2005). The economic burden of depression in the US: societal and patient perspectives. Expert Opinion on Pharmacotherapy, 6, 369.

    Article  PubMed  Google Scholar 

  • Gunten, A. V., Fox, N. C., Cipolotti, L., & Ron, M. A. (2000). A Volumetric Study of Hippocampus and Amygdala in Depressed Patients With Subjective Memory Problems. Journal of Neuropsychiatry & Clinical Neurosciences, 12, 493.

    Article  Google Scholar 

  • Hamilton, J. P., Siemer, M., & Gotlib, I. H. (2008). Amygdala volume in Major Depressive Disorder: A meta-analysis of magnetic resonance imaging studies. Molecular Psychiatry, 13, 993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasin, D. S., Goodwin, R. D., Stinson, F. S., & Grant, B. F. (2005). Epidemiology of major depressive disorder: results from the National Epidemiologic Survey on Alcoholism and Related Conditions. Archives of General Psychiatry, 62, 1097–1106. https://doi.org/10.1001/archpsyc.62.10.1097.

    Article  PubMed  Google Scholar 

  • Hastings, R. S., Parsey, R. V., Oquendo, M. A., Arango, V., & Mann, J. J. (2004). Volumetric analysis of the prefrontal cortex, amygdala, and hippocampus in major depression. Neuropsychopharmacology Official Publication of the American College of. Neuropsychopharmacology, 29, 952.

    Article  PubMed  Google Scholar 

  • Heller, A. S., et al. (2009). Reduced Capacity to Sustain Positive Emotion in Major Depression Reflects Diminished Maintenance of Fronto-Striatal Brain Activation. Proceedings of the National Academy of Sciences of the United States of America, 106, 22445–22450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hickie, I., et al. (2005). Reduced hippocampal volumes and memory loss in patients with early- and late-onset depression. British Journal of Psychiatry, 186, 197–202.

    Article  Google Scholar 

  • Hitti, F. L., & Siegelbaum, S. A. (2014). The hippocampal CA2 region is essential for social memory. Nature, 508, 88–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hotelling, H. (1992). The Generalization of Student's Ratio. Springer New York.

  • Joshi, S. H., et al. (2016). Structural Plasticity of the Hippocampus and Amygdala Induced by Electroconvulsive Therapy in Major Depression. Biological Psychiatry, 79, 282–292.

    Article  PubMed  Google Scholar 

  • Kessler, R. C., et al. (2003). The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). Jama, 289, 3095.

    Article  PubMed  Google Scholar 

  • Kessler, R. C., Berglund, P., Demler, O., Jin, R., Merikangas, K. R., & Walters, E. E. (2005). Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. BMC Complementary and Alternative Medicine, 14, 422–422.

    Google Scholar 

  • Krishnan, V., & Nestler, E. J. (2008). The molecular neurobiology of depression. Nature, 455, 894–902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kronenberg, G., Tebartz, v E L., Regen, F., Deuschle, M., Heuser, I., & Colla, M. (2009). Reduced amygdala volume in newly admitted psychiatric in-patients with unipolar major depression. Journal of Psychiatric Research, 43, 1112–1117.

    Article  PubMed  Google Scholar 

  • Lange, C., & Irle, E. (2004). Enlarged amygdala volume and reduced hippocampal volume in young women with major depression. Psychological Medicine, 34, 1059–1064.

    Article  CAS  PubMed  Google Scholar 

  • Lao, Y., Wang, Y., Shi, J., Ceschin, R., Nelson, M. D., Panigrahy, A., & Leporé, N. (2016). Thalamic alterations in preterm neonates and their relation to ventral striatum disturbances revealed by a combined shape and pose analysis. Brain Structure & Function, 221, 487–506.

    Article  Google Scholar 

  • Ledoux, J. E., Cicchetti, P., Xagoraris, A., & Romanski, L. M. (1990). The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 10, 1062–1069.

    Article  CAS  Google Scholar 

  • Lemogne, C., et al. (2006). Episodic autobiographical memory in depression: Specificity, autonoetic consciousness, and self-perspective. Consciousness and Cognition, 15, 258–268.

    Article  PubMed  Google Scholar 

  • Lepage, M., Habib, R., & Tulving, E. (2015). Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus, 8, 313–322.

    Article  Google Scholar 

  • Lepore, N., et al. (2008). Generalized Tensor-Based Morphometry of HIV/AIDS Using Multivariate Statistics on Deformation Tensors. IEEE Transactions on Medical Imaging, 27, 129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lesch, K. P. (2004). Gene–environment interaction and the genetics of depression. Journal of Psychiatry & Neuroscience Jpn, 29, 174–184.

    Google Scholar 

  • Linden, D. J., & Connor, J. A. (2003). Long-term synaptic depression. Annual Review of Neuroscience, 18, 319–357.

    Article  Google Scholar 

  • Liverant, G. I., Brown, T. A., Barlow, D. H., & Roemer, L. (2008). Emotion regulation in unipolar depression: the effects of acceptance and suppression of subjective emotional experience on the intensity and duration of sadness and negative affect. Behaviour Research and Therapy, 46, 1201–1209.

    Article  PubMed  Google Scholar 

  • Lucassen, P. J., et al. (2006) Stress, depression and hippocampal apoptosis. CNS & Neurological Disorders - Drug Targets (Formerly Current Drug Targets - CNS & Neurological Disorders), 5, 531–546.

  • Maller, J. J., Daskalakis, Z. J., & Fitzgerald, P. B. (2007). Hippocampal volumetrics in depression: the importance of the posterior tail. Hippocampus, 17, 1023–1027.

    Article  PubMed  Google Scholar 

  • Malykhin, N. V., Carter, R., Seres, P., & Coupland, N. J. (2010). Structural changes in the hippocampus in major depressive disorder: contributions of disease and treatment. Journal of Psychiatry & Neuroscience Jpn, 35, 337.

    Article  Google Scholar 

  • Marcus DBM, Yasamy MT, Ommeren MV, Saxena S, Dan C (2012) A Global Public Health Concern

  • Mervaala, E., et al. (2000). Quantitative MRI of the hippocampus and amygdala in severe depression. Psychological Medicine, 30, 117–125.

    Article  CAS  PubMed  Google Scholar 

  • Mormino, E. C., et al. (2009). Episodic memory loss is related to hippocampal-mediated β-amyloid deposition in elderly subjects. Brain, 132, 1310–1323.

    Article  CAS  PubMed  Google Scholar 

  • Morris, J. S., Öhman, A., & Dolan, R. J. (1998). Conscious and unconscious emotional learning in the human amygdala. Nature, 393, 467–470.

    Article  CAS  PubMed  Google Scholar 

  • Moser, M. B., & Moser, E. I. (2015). Functional differentiation in the hippocampus. Hippocampus, 8, 608–619.

    Article  Google Scholar 

  • Neumeister, A., et al. (2005). Reduced hippocampal volume in unmedicated, remitted patients with major depression versus control subjects. Biological Psychiatry, 57, 935–937.

    Article  PubMed  Google Scholar 

  • Nho, K., et al. (2015). Comprehensive Gene- and Pathway-Based Analysis of Depressive Symptoms in Older Adults. Journal of Alzheimers Disease Jad, 45, 1197–1206.

    Article  CAS  PubMed  Google Scholar 

  • Nichols, T. E., & Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping, 15, 1–25.

    Article  PubMed  Google Scholar 

  • Phelps, E. A., O'Connor, K. J., Gatenby, J. C., Gore, J. C., Grillon, C., & Davis, M. (2001). Activation of the left amygdala to a cognitive representation of fear. Nature Neuroscience, 4, 437–441.

    Article  CAS  PubMed  Google Scholar 

  • Pizer, S. M., Fritsch, D. S., Yushkevich, P. A., Johnson, V. E., & Chaney, E. L. (1999). Segmentation, registration, and measurement of shape variation via image object shape. IEEE Transactions on Medical Imaging, 18, 851–865.

    Article  CAS  PubMed  Google Scholar 

  • Posener, J. A., et al. (2003). High-dimensional mapping of the hippocampus in depression. American Journal of Psychiatry, 160(83).

  • Price, J. L., & Drevets, W. C. (2012). Neural circuits underlying the pathophysiology of mood disorders. Trends in Cognitive Sciences, 16, 61–71.

    Article  PubMed  Google Scholar 

  • Reagh, Z. M., Noche, J. A., Tustison, N. J., Delisle, D., Murray, E. A., & Yassa, M. A. (2018). Functional Imbalance of Anterolateral Entorhinal Cortex and Hippocampal Dentate/CA3&nbsp. Underlies Age-Related Object Pattern Separation Deficits, 97, 1187–1198 e1184.

    CAS  Google Scholar 

  • Rodrigues, S. M., Schafe, G. E., & Ledoux, J. E. (2004). Molecular Mechanisms Underlying Emotional Learning and Memory in the Lateral Amygdala. Neuron, 44, 75.

    Article  CAS  PubMed  Google Scholar 

  • Root, C. M., Denny, C. A., Hen, R., & Axel, R. (2014). The participation of cortical amygdala in innate, odour-driven behaviour. Nature, 515, 269–273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosso, I. M., Cintron, C. M., Steingard, R. J., Renshaw, P. F., Young, A. D., & Yurgeluntodd, D. A. (2005). Amygdala and hippocampus volumes in pediatric major depression. Biological Psychiatry, 57, 21–26.

    Article  PubMed  Google Scholar 

  • Saleh, K., Carballedo, A., Lisiecka, D., Fagan, A. J., Connoly, G., Boyle, G., & Frodl, T. (2012). Impact of family history and depression on amygdala volume. Psychiatry Research. Neuroimaging, 203, 24–30.

    Article  PubMed  Google Scholar 

  • Saxe, M. D., et al. (2007). Paradoxical Influence of Hippocampal Neurogenesis on Working Memory. Proceedings of the National Academy of Sciences of the United States of America, 104, 4642–4646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmaal, L., et al. (2016). Subcortical brain alterations in major depressive disorder: findings from the ENIGMA Major Depressive Disorder working group. Molecular Psychiatry, 21, 806–812.

    Article  CAS  PubMed  Google Scholar 

  • Schmaal, L., et al. (2017). Cortical abnormalities in adults and adolescents with major depression based on brain scans from 20 cohorts worldwide in the ENIGMA Major Depressive Disorder Working Group. Molecular Psychiatry, 22, 900.

    Article  CAS  PubMed  Google Scholar 

  • Schnittker, J. (2010). Gene-environment correlations in the stress-depression relationship. Journal of Health and Social Behavior, 51, 229.

    Article  PubMed  Google Scholar 

  • Shammah-Lagnado, S. J., Alheid, G. F., & Heimer, L. (1999). Afferent connections of the interstitial nucleus of the posterior limb of the anterior commissure and adjacent amygdalostriatal transition area in the rat. Neuroscience, 94, 1097–1123.

    Article  CAS  PubMed  Google Scholar 

  • Sheline, Y. I., Wang, P. W., Gado, M. H., Csernansky, J. G., & Vannier, M. W. (1996). Hippocampal atrophy in recurrent major depression. Proceedings of the National Academy of Sciences of the United States of America, 93, 3908–3913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheline, Y. I., Gado, M. H., & Price, J. L. (1998). Amygdala core nuclei volumes are decreased in recurrent major depression. Neuroreport, 9, 2023–2028.

    Article  CAS  PubMed  Google Scholar 

  • Shi, J., Thompson, P. M., Gutman, B., & Wang, Y. (2013). Surface fluid registration of conformal representation: application to detect disease burden and genetic influence on hippocampus. Neuroimage, 78, 111.

    Article  PubMed  Google Scholar 

  • Shi, J., et al. (2015). Studying ventricular abnormalities in mild cognitive impairment with hyperbolic Ricci flow and tensor-based morphometry. Neuroimage, 104, 1–20.

    Article  PubMed  Google Scholar 

  • Silk, J. S., Steinberg, L., & Morris, A. S. (2003). Adolescents' emotion regulation in daily life: links to depressive symptoms and problem behavior. Child Development, 74, 1869–1880.

    Article  PubMed  Google Scholar 

  • Smith, D. M., & Mizumori, S. J. (2006). Hippocampal place cells, context, and episodic memory. Hippocampus, 16, 716–729.

    Article  PubMed  Google Scholar 

  • Snyder, H. R. (2013). Major depressive disorder is associated with broad impairments on neuropsychological measures of executive function: A meta-analysis and review. Psychological Bulletin, 139, 81–132.

    Article  PubMed  Google Scholar 

  • Styner, M., et al. (2006). Framework for the Statistical Shape Analysis of Brain Structures using SPHARM-PDM. Insight Journal, 1071, 242.

    Google Scholar 

  • Sullivan, P. F., Neale, M. C., & Kendler, K. S. (2000). Genetic Epidemiology of Major Depression: Review and Meta-Analysis. American Journal of Psychiatry, 157, 1552.

    Article  CAS  PubMed  Google Scholar 

  • Sun, Q., Sotayo, A., Cazzulino, A. S., Snyder, A. M., Denny, C. A., & Siegelbaum, S. A. (2017). Proximodistal heterogeneity of hippocampal CA3 pyramidal neuron intrinsic properties, connectivity, and reactivation during memory recall. Neuron, 95, 656–672 e653.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, Y., et al. (2007). Reduced ventral anterior cingulate and amygdala volumes in medication-naïve females with major depressive disorder: A voxel-based morphometric magnetic resonance imaging study. Psychiatry Research, 156, 83.

    Article  PubMed  Google Scholar 

  • Thompson, P., Giedd, J. N., Woods, R. P., Macdonald, D., Evans, A. C., & Toga, A. W. (2000). Growth patterns in the developing human brain detected using continuum-mechanical tensor mapping. Nature, 404, 190–193.

    Article  CAS  PubMed  Google Scholar 

  • Thompson, P. M., et al. (2003). Dynamics of Gray Matter Loss in Alzheimer's Disease. Journal of Neuroscience the Official Journal of the Society for. Neuroscience, 23, 994–1005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson, P. M., et al. (2004). Mapping hippocampal and ventricular change in Alzheimer disease. Neuroimage, 22, 1754–1766.

    Article  PubMed  Google Scholar 

  • Tulving, E., & Markowitsch, H. J. (1998). Episodic and declarative memory: role of the hippocampus. Hippocampus, 8, 198.

    Article  CAS  PubMed  Google Scholar 

  • Uher, R. (2008). The implications of gene-environment interactions in depression: will cause inform cure? Molecular Psychiatry, 13, 1070–1078.

    Article  CAS  PubMed  Google Scholar 

  • Van, E. P., et al. (2009). Amygdala volume marks the acute state in the early course of depression. Biological Psychiatry, 65, 812–818.

    Article  Google Scholar 

  • Videbech, P., & Ravnkilde, B. (2004). Hippocampal volume and depression: a meta-analysis of MRI studies. American Journal of Psychiatry, 161, 1957–1966.

    Article  PubMed  Google Scholar 

  • Viskontas, I. V., Carr, V. A., Engel, S. A., & Knowlton, B. J. (2009). The neural correlates of recollection: hippocampal activation declines as episodic memory fades. Hippocampus, 19, 265–272.

    Article  PubMed  Google Scholar 

  • Wang Y, Gu X, Chan TF, Thompson PM. (2008). Yau ST Conformal slit mapping and its applications to brain surface parameterization. In International conference on medical image computing and computer-assisted intervention (pp. 585-593).

  • Wang Y, Chan TF, Toga AW. (2009) Thompson PM Multivariate Tensor-Based Brain Anatomical Surface Morphometry via Holomorphic One-Forms. In International conference on medical image computing & computer-assisted intervention (pp. 337-344)

  • Wang, P. S., Simon, G., & Kessler, R. C. (2010). The economic burden of depression and the cost-effectiveness of treatment. International Journal of Methods in Psychiatric Research, 12, 22–33.

    Article  Google Scholar 

  • Wang, Y., et al. (2011). Surface-based TBM boosts power to detect disease effects on the brain: An N = 804 ADNI study ☆. Neuroimage, 56, 1993–2010.

    Article  PubMed  Google Scholar 

  • Wang Y et al. (2013) Surface multivariate tensor-based morphometry on premature neonates: A pilot study

  • Wang, Y., et al. (2013a). Applying tensor-based morphometry to parametric surfaces can improve MRI-based disease diagnosis. Neuroimage, 74, 209–230.

    Article  PubMed  Google Scholar 

  • Wang Y, Panigrahy A, Ceschin R, Liu S, Thompson PM, Leporé N (2013b) Surface morphometry of subcortical structures in premature neonates

  • Williams, J. B. (1988). A structured interview guide for the Hamilton Depression Rating Scale. Archives of General Psychiatry, 45, 742.

    Article  CAS  PubMed  Google Scholar 

  • Williams, J. B. (2001). Standardizing the Hamilton Depression Rating Scale: past, present, and future. European Archives of Psychiatry and Clinical Neuroscience, 251(Suppl 2), II6.

    Article  PubMed  Google Scholar 

  • Williams, J. M., & Broadbent, K. (1986). Autobiographical memory in suicide attempters. Journal of Abnormal Psychology, 95, 144.

    Article  CAS  PubMed  Google Scholar 

  • Williams, J. M., & Scott, J. (1988). Autobiographical memory in depression. Psychological Medicine, 18, 689.

    Article  CAS  PubMed  Google Scholar 

  • Winocur, G., Wojtowicz, J. M., Sekeres, M., Snyder, J. S., & Wang, S. (2006). Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus, 16, 296.

    Article  PubMed  Google Scholar 

  • Wood, E. R., Dudchenko, P. A., & Eichenbaum, H. (1999). The global record of memory in hippocampal neuronal activity. Nature, 397, 613.

    Article  CAS  PubMed  Google Scholar 

  • Woods, R. P. (2003). Characterizing volume and surface deformations in an atlas framework: theory, applications, and implementation. Neuroimage, 18, 769.

    Article  PubMed  Google Scholar 

  • Yoshimura, S., Ueda, K., Suzuki, S., Onoda, K., Okamoto, Y., & Yamawaki, S. (2009). Self-referential processing of negative stimuli within the ventral anterior cingulate gyrus and right amygdala. Brain and Cognition, 69, 218–225.

    Article  PubMed  Google Scholar 

  • Zald, D. H. (2003). The human amygdala and the emotional evaluation of sensory stimuli. Brain Research. Brain Research Reviews, 41, 88–123.

    Article  PubMed  Google Scholar 

  • Zeineh, M. M., Engel, S. A., Thompson, P. M., & Bookheimer, S. Y. (2003). Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science, 299, 577–580.

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by the National Basic Research Program of China (973 Program) (No.2014CB744600), the National Natural Science Foundation of China (Grant No.61210010, No.61632014 and No.61571047), the Program of International S&T Cooperation of MOST (No.2013DFA11140), the Program of Beijing Municipal Science & Technology Commission (No.Z171100000117005), the National Key Research and Development Program of China (No.2016YFC1307203) and the Fundamental Research Funds for the Central Universities (lzujbky-2017-kb08).

Author information

Authors and Affiliations

  1. School of Information Science and Engineering, Lanzhou University, P.O. Box 730000, Lanzhou, China

    Zhijun Yao, Yu Fu, Yue Yu, Zicheng Zhang & Bin Hu

  2. School of Computing, Informatics, and Decision Systems Engineering, Arizona State University, P.O. Box 878809, Tempe, AZ, 85287, USA

    Jianfeng Wu & Yalin Wang

  3. Department of Radiology, Gansu Provincial Hospital, Lanzhou, China

    Wenwen Zhang

  4. State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, China

    Xia Wu

  5. College of Information Science and Technology, Beijing Normal University, P.O. Box 100000, Beijing, China

    Xia Wu

Authors
  1. Zhijun Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianfeng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wenwen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yue Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zicheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xia Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yalin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xia Wu, Yalin Wang or Bin Hu.

Ethics declarations

Conflict of interest

All authors declared no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.

Informed consent

Informed written consents were obtained from all individual participants included in the study.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yao, Z., Fu, Y., Wu, J. et al. Morphological changes in subregions of hippocampus and amygdala in major depressive disorder patients. Brain Imaging and Behavior 14, 653–667 (2020). https://doi.org/10.1007/s11682-018-0003-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-018-0003-1

Keywords

Search

Navigation