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Anterior hippocampal dysfunction in early psychosis: a 2-year follow-up study

Published online by Cambridge University Press:  20 April 2021

Maureen McHugo*
Affiliation:
Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
Suzanne Avery
Affiliation:
Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
Kristan Armstrong
Affiliation:
Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
Baxter P. Rogers
Affiliation:
Vanderbilt University Institute of Imaging Sciences, Nashville, TN, USA
Simon N. Vandekar
Affiliation:
Department of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA
Neil D. Woodward
Affiliation:
Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
Jennifer Urbano Blackford
Affiliation:
Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, TN, USA Research and Development, Tennessee Valley Healthcare System, United States Department of Veteran Affairs, Nashville, TN, USA
Stephan Heckers
Affiliation:
Department of Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, TN, USA
*
Author for correspondence: Maureen McHugo, E-mail: maureen.mchugo@vanderbilt.edu

Abstract

Background

Cross-sectional studies indicate that hippocampal function is abnormal across stages of psychosis. Neural theories of psychosis pathophysiology suggest that dysfunction worsens with illness stage. Here, we test the hypothesis that hippocampal function is impaired in the early stage of psychosis and declines further over the next 2 years.

Methods

We measured hippocampal function over 2 years using a scene processing task in 147 participants (76 individuals in the early stage of a non-affective psychotic disorder and 71 demographically similar healthy control individuals). Two-year follow-up was completed in 97 individuals (50 early psychosis, 47 healthy control). Voxelwise longitudinal analysis of activation in response to scenes was carried out within a hippocampal region of interest to test for group differences at baseline and a group by time interaction.

Results

At baseline, we observed lower anterior hippocampal activation in the early psychosis group relative to the healthy control group. Contrary to our hypothesis, hippocampal activation remained consistent and did not show the predicted decline over 2 years in the early psychosis group. Healthy controls showed a modest reduction in hippocampal activation after 2 years.

Conclusions

The results of this study suggest that hippocampal dysfunction in early psychosis does not worsen over 2 years and highlight the need for longer-term longitudinal studies.

Type
Original Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Achim, A. M., Bertrand, M.-C., Sutton, H., Montoya, A., Czechowska, Y., Malla, A. K., … Lepage, M. (2007). Selective abnormal modulation of hippocampal activity during memory formation in first-episode psychosis. Archives of General Psychiatry, 64(9), 9991014. doi:10.1001/archpsyc.64.9.999.CrossRefGoogle ScholarPubMed
Achim, A. M., & Lepage, M. (2005). Episodic memory-related activation in schizophrenia: Meta-analysis. The British Journal of Psychiatry: The Journal of Mental Science, 187, 500509. doi:10.1192/bjp.187.6.500.CrossRefGoogle ScholarPubMed
Aleman, A., Hijman, R., de Haan, E. H., & Kahn, R. S. (1999). Memory impairment in schizophrenia: A meta-analysis. The American Journal of Psychiatry, 156(9), 13581366. doi:10.1176/ajp.156.9.1358.CrossRefGoogle ScholarPubMed
Allen, P., Chaddock, C. A., Egerton, A., Howes, O. D., Bonoldi, I., Zelaya, F., … McGuire, P. (2016). Resting hyperperfusion of the hippocampus, midbrain, and basal ganglia in people at high risk for psychosis. The American Journal of Psychiatry, 173(4), 392399. doi:10.1176/appi.ajp.2015.15040485.CrossRefGoogle ScholarPubMed
Aly, M., & Turk-Browne, N. B. (2017). How hippocampal memory shapes, and is shaped by, attention. In Hannula, D. E. & Duff, M. C. (Eds.), The hippocampus from cells to systems: Structure, connectivity, and functional contributions to memory and flexible cognition (pp. 369403). Cham: Springer International Publishing. doi:10.1007/978-3-319-50406-3_12.CrossRefGoogle Scholar
Anderson, M. C., Bunce, J. G., & Barbas, H. (2016). Prefrontal-hippocampal pathways underlying inhibitory control over memory. Neurobiology of Learning and Memory, 134(Pt A), 145161. doi:10.1016/j.nlm.2015.11.008.CrossRefGoogle ScholarPubMed
Armstrong, K., Avery, S., Blackford, J. U., Woodward, N., & Heckers, S. (2018). Impaired associative inference in the early stage of psychosis. Schizophrenia Research, 202, 8690. doi:10.1016/j.schres.2018.06.049.CrossRefGoogle ScholarPubMed
Avery, S. N., Armstrong, K., McHugo, M., Vandekar, S., Blackford, J. U., Woodward, N. D., … Heckers, S. (2021). Relational memory in the early stage of psychosis: A 2-year follow-up study. Schizophrenia Bulletin, 47(1), 7586. 10.1093/schbul/sbaa081.CrossRefGoogle ScholarPubMed
Avery, S. N., McHugo, M., Armstrong, K., Blackford, J. U., Vandekar, S., Woodward, N. D., & Heckers, S. (2020b). Habituation during encoding: A new approach to the evaluation of memory deficits in schizophrenia. Schizophrenia Research, 223, 179185. doi:10.1016/j.schres.2020.07.007.CrossRefGoogle Scholar
Avery, S. N., McHugo, M., Armstrong, K., Blackford, J. U., Woodward, N. D., & Heckers, S. (2019). Disrupted habituation in the early stage of psychosis. Biological Psychiatry. Cognitive Neuroscience and Neuroimaging, 4(11), 10041012. doi:10.1016/j.bpsc.2019.06.007.CrossRefGoogle ScholarPubMed
Avery, S. N., McHugo, M., Armstrong, K., Blackford, J. U., Woodward, N. D., & Heckers, S. (2021). Stable habituation deficits in the early stage of psychosis: A 2-year follow-up study. Translational Psychiatry, 11(1), 20. doi:10.1038/s41398-020-01167-9.CrossRefGoogle ScholarPubMed
Bennett, C. M., & Miller, M. B. (2010). How reliable are the results from functional magnetic resonance imaging? Annals of the New York Academy of Sciences, 1191, 133155. doi:10.1111/j.1749-6632.2010.05446.x.CrossRefGoogle ScholarPubMed
Bergé, D., Carmona, S., Salgado, P., Rovira, M., Bulbena, A., & Vilarroya, O. (2014). Limbic activity in antipsychotic naïve first-episode psychotic subjects during facial emotion discrimination. European Archives of Psychiatry and Clinical Neuroscience, 264(4), 271283. doi:10.1007/s00406-013-0465-5.CrossRefGoogle ScholarPubMed
Blessing, E. M., Murty, V. P., Zeng, B., Wang, J., Davachi, L., & Goff, D. C. (2020). Anterior hippocampal-cortical functional connectivity distinguishes antipsychotic naïve first-episode psychosis patients from controls and may predict response to second-generation antipsychotic treatment. Schizophrenia Bulletin, 46(3), 680689. doi:10.1093/schbul/sbz076.CrossRefGoogle ScholarPubMed
Blockley, N. P., Griffeth, V. E. M., Simon, A. B., & Buxton, R. B. (2013). A review of calibrated blood oxygenation level-dependent (BOLD) methods for the measurement of task-induced changes in brain oxygen metabolism. NMR in Biomedicine, 26(8), 9871003. doi:10.1002/nbm.2847.CrossRefGoogle ScholarPubMed
Bolding, M. S., White, D. M., Hadley, J. A., Weiler, M., Holcomb, H. H., & Lahti, A. C. (2012). Antipsychotic drugs alter functional connectivity between the medial frontal cortex, hippocampus, and nucleus accumbens as measured by H215O PET. Frontiers in Psychiatry, 3, 105. doi:10.3389/fpsyt.2012.00105.CrossRefGoogle ScholarPubMed
Cadena, E. J., White, D. M., Kraguljac, N. V., Reid, M. A., Maximo, J. O., Nelson, E. A., … Lahti, A. C. (2018). A longitudinal multimodal neuroimaging study to examine relationships between resting state glutamate and task related BOLD response in schizophrenia. Frontiers in Psychiatry, 9, 632. doi:10.3389/fpsyt.2018.00632.CrossRefGoogle ScholarPubMed
Cave, C. B. (1997). Very long-lasting priming in picture naming. Psychological Science, 8(4), 322325. doi:10.1111/j.1467-9280.1997.tb00446.x.CrossRefGoogle Scholar
Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the USA, 113(28), 79007905. doi:10.1073/pnas.1602413113.CrossRefGoogle ScholarPubMed
Elliott, M. L., Knodt, A. R., Cooke, M., Kim, M. J., Melzer, T. R., Keenan, R., … Hariri, A. R. (2019). General functional connectivity: Shared features of resting-state and task fMRI drive reliable and heritable individual differences in functional brain networks. NeuroImage, 189, 516532. doi:10.1016/j.neuroimage.2019.01.068.CrossRefGoogle ScholarPubMed
Elliott, M. L., Knodt, A. R., Ireland, D., Morris, M. L., Poulton, R., Ramrakha, S., … Hariri, A. R. (2020). What is the test-retest reliability of common task-functional MRI measures? New empirical evidence and a meta-analysis. Psychological Science, 31(7), 792806. doi:10.1177/0956797620916786.CrossRefGoogle ScholarPubMed
Fanselow, M. S., & Dong, H.-W. (2010). Are the dorsal and ventral hippocampus functionally distinct structures? Neuron, 65(1), 719. doi:10.1016/j.neuron.2009.11.031.CrossRefGoogle ScholarPubMed
First, M., Spitzer, R., Miriam, G., & Williams, J. (2002). Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition with psychotic screen (SCID-I/P W/PSY SCREEN). New York, NY: Biometrics Research, New York State Psychiatric Institute.Google Scholar
Francis, M. M., Hummer, T. A., Vohs, J. L., Yung, M. G., Liffick, E., Mehdiyoun, N. F., … Breier, A. (2016). Functional neuroanatomical correlates of episodic memory impairment in early phase psychosis. Brain Imaging and Behavior, 10(1), 111. doi:10.1007/s11682-015-9357-9.CrossRefGoogle ScholarPubMed
Gardner, D. M., Murphy, A. L., O'Donnell, H., Centorrino, F., & Baldessarini, R. J. (2010). International consensus study of antipsychotic dosing. The American Journal of Psychiatry, 167(6), 686693. doi:10.1176/appi.ajp.2009.09060802.CrossRefGoogle ScholarPubMed
González-Vivas, C., Soldevila-Matías, P., Sparano, O., García-Martí, G., Martí-Bonmatí, L., Crespo-Facorro, B., … Sanjuan, J. (2019). Longitudinal studies of functional magnetic resonance imaging in first-episode psychosis: A systematic review. European Psychiatry: The Journal of the Association of European Psychiatrists, 59, 6069. doi:10.1016/j.eurpsy.2019.04.009.CrossRefGoogle ScholarPubMed
Grace, A. A. (2016). Dysregulation of the dopamine system in the pathophysiology of schizophrenia and depression. Nature Reviews. Neuroscience, 17(8), 524532. doi:10.1038/nrn.2016.57.CrossRefGoogle ScholarPubMed
Guillaume, B., Hua, X., Thompson, P. M., Waldorp, L., Nichols, T. E., & Alzheimer's Disease Neuroimaging Initiative, . (2014). Fast and accurate modelling of longitudinal and repeated measures neuroimaging data. NeuroImage, 94, 287302. doi:10.1016/j.neuroimage.2014.03.029.CrossRefGoogle ScholarPubMed
Guillaume, B., Nichols, T. E., & ADNI, (2015). Non-parametric inference for longitudinal and repeated-measures neuroimaging data with the wild bootstrap. Organization for Human Brain Mapping. figshare. doi:https://doi.org/10.6084/M9.FIGSHARE.5478229.V1.CrossRefGoogle Scholar
Gurler, D., White, D. M., Kraguljac, N. V., Ver Hoef, L., Martin, C., Tennant, B., … Lahti, A. C. (2020). Neural signatures of memory encoding in schizophrenia are modulated by antipsychotic treatment. Neuropsychobiology, 80(1), 1224. doi:10.1159/000506402.CrossRefGoogle ScholarPubMed
Haukvik, U. K., Hartberg, C. B., Nerland, S., Jørgensen, K. N., Lange, E. H., Simonsen, C., … Agartz, I. (2016). No progressive brain changes during a 1-year follow-up of patients with first-episode psychosis. Psychological Medicine, 46(3), 589598. doi:10.1017/S003329171500210X.CrossRefGoogle ScholarPubMed
Heckers, S., & Konradi, C. (2015). GABAergic mechanisms of hippocampal hyperactivity in schizophrenia. Schizophrenia Research, 167(1–3), 411. doi:10.1016/j.schres.2014.09.041.CrossRefGoogle ScholarPubMed
Heckers, S., Rauch, S. L., Goff, D., Savage, C. R., Schacter, D. L., Fischman, A. J., & Alpert, N. M. (1998). Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nature Neuroscience, 1(4), 318323. doi:10.1038/1137.CrossRefGoogle ScholarPubMed
Hedge, C., Powell, G., & Sumner, P. (2018). The reliability paradox: Why robust cognitive tasks do not produce reliable individual differences. Behavior Research Methods, 50(3), 11661186. doi:10.3758/s13428-017-0935-1.CrossRefGoogle Scholar
Ho, N. F., Holt, D. J., Cheung, M., Iglesias, J. E., Goh, A., Wang, M., … Zhou, J. (2017a). Progressive decline in hippocampal CA1 volume in individuals at ultra-high-risk for psychosis who do not remit: Findings from the longitudinal youth at risk study. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 42(6), 13611370. doi:10.1038/npp.2017.5.CrossRefGoogle Scholar
Ho, N. F., Iglesias, J. E., Sum, M. Y., Kuswanto, C. N., Sitoh, Y. Y., De Souza, J., … Holt, D. J. (2017b). Progression from selective to general involvement of hippocampal subfields in schizophrenia. Molecular Psychiatry, 22(1), 142152. doi:10.1038/mp.2016.4.CrossRefGoogle ScholarPubMed
Hodgetts, C. J., Shine, J. P., Lawrence, A. D., Downing, P. E., & Graham, K. S. (2016). Evidencing a place for the hippocampus within the core scene processing network. Human Brain Mapping, 37(11), 37793794. doi:10.1002/hbm.23275.CrossRefGoogle ScholarPubMed
Holt, D. J. (2019). Deficient hippocampal habituation in psychosis: A manifestation of hippocampal overactivity? Biological Psychiatry. Cognitive Neuroscience and Neuroimaging, 4(11), 938939. doi:10.1016/j.bpsc.2019.09.002.CrossRefGoogle ScholarPubMed
Holt, D. J., Weiss, A. P., Rauch, S. L., Wright, C. I., Zalesak, M., Goff, D. C., … Heckers, S. (2005). Sustained activation of the hippocampus in response to fearful faces in schizophrenia. Biological Psychiatry, 57(9), 10111019. doi:10.1016/j.biopsych.2005.01.033.CrossRefGoogle ScholarPubMed
Kawasaki, Y., Suzuki, M., Maeda, Y., Urata, K., Yamaguchi, N., Matsuda, H., … Takashima, T. (1992). Regional cerebral blood flow in patients with schizophrenia. A preliminary report. European Archives of Psychiatry and Clinical Neuroscience, 241(4), 195200. doi:10.1007/BF02190252.CrossRefGoogle ScholarPubMed
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin, 13(2), 261276. doi:10.1093/schbul/13.2.261.CrossRefGoogle ScholarPubMed
Khalili-Mahani, N., Rombouts, S. A. R. B., van Osch, M. J. P., Duff, E. P., Carbonell, F., Nickerson, L. D., … van Gerven, J. M. (2017). Biomarkers, designs, and interpretations of resting-state fMRI in translational pharmacological research: A review of state-of-the-art, challenges, and opportunities for studying brain chemistry. Human Brain Mapping, 38(4), 22762325. doi:10.1002/hbm.23516.CrossRefGoogle ScholarPubMed
Kim, H. (2017). Brain regions that show repetition suppression and enhancement: A meta-analysis of 137 neuroimaging experiments. Human Brain Mapping, 38(4), 18941913. doi:10.1002/hbm.23492.CrossRefGoogle ScholarPubMed
Kovács, G., Grotheer, M., Münke, L., Kéri, S., & Nenadić, I. (2019). Significant repetition probability effects in schizophrenia. Psychiatry Research. Neuroimaging, 290, 2229. doi:10.1016/j.pscychresns.2019.05.006.CrossRefGoogle ScholarPubMed
Kragel, P., Han, X., Kraynak, T., Gianaros, P. J., & Wager, T. (2020). fMRI can be highly reliable, but it depends on what you measure. PsyArXiv. doi:10.31234/osf.io/9eaxk.CrossRefGoogle Scholar
Lahti, A. C., Holcomb, H. H., Weiler, M. A., Medoff, D. R., & Tamminga, C. A. (2003). Functional effects of antipsychotic drugs: Comparing clozapine with haloperidol. Biological Psychiatry, 53(7), 601608. doi:10.1016/s0006-3223(02)01602-5.CrossRefGoogle ScholarPubMed
Lahti, A. C., Weiler, M. A., Holcomb, H. H., Tamminga, C. A., & Cropsey, K. L. (2009). Modulation of limbic circuitry predicts treatment response to antipsychotic medication: A functional imaging study in schizophrenia. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 34(13), 26752690. doi:10.1038/npp.2009.94.CrossRefGoogle ScholarPubMed
Larsen, K. M., Mørup, M., Birknow, M. R., Fischer, E., Olsen, L., Didriksen, M., … Siebner, H. R. (2019). Individuals with 22q11.2 deletion syndrome show intact prediction but reduced adaptation in responses to repeated sounds: Evidence from Bayesian mapping. NeuroImage. Clinical, 22, 101721. doi:10.1016/j.nicl.2019.101721.CrossRefGoogle ScholarPubMed
Lee, J., Reavis, E. A., Engel, S. A., Altshuler, L. L., Cohen, M. S., Glahn, D. C., … Green, M. F. (2019). fMRI evidence of aberrant neural adaptation for objects in schizophrenia and bipolar disorder. Human Brain Mapping, 40(5), 16081617. doi:10.1002/hbm.24472.CrossRefGoogle ScholarPubMed
Leucht, S., Samara, M., Heres, S., Patel, M. X., Woods, S. W., & Davis, J. M. (2014). Dose equivalents for second-generation antipsychotics: The minimum effective dose method. Schizophrenia Bulletin, 40(2), 314326. doi:10.1093/schbul/sbu001.CrossRefGoogle ScholarPubMed
Liddle, P. F., Lane, C. J., & Ngan, E. T. (2000). Immediate effects of risperidone on cortico-striato-thalamic loops and the hippocampus. The British Journal of Psychiatry: The Journal of Mental Science, 177, 402407. doi:10.1192/bjp.177.5.402.CrossRefGoogle ScholarPubMed
Lieberman, J. A., Girgis, R. R., Brucato, G., Moore, H., Provenzano, F., Kegeles, L., … Small, S. A. (2018). Hippocampal dysfunction in the pathophysiology of schizophrenia: A selective review and hypothesis for early detection and intervention. Molecular Psychiatry, 23(8), 17641772. doi:10.1038/mp.2017.249.CrossRefGoogle ScholarPubMed
Makowski, C., Bodnar, M., Shenker, J. J., Malla, A. K., Joober, R., Chakravarty, M. M., & Lepage, M. (2017). Linking persistent negative symptoms to amygdala-hippocampus structure in first-episode psychosis. Translational Psychiatry, 7(8), e1195. doi:10.1038/tp.2017.168.CrossRefGoogle ScholarPubMed
Malaspina, D., Harkavy-Friedman, J., Corcoran, C., Mujica-Parodi, L., Printz, D., Gorman, J. M., & Van Heertum, R. (2004). Resting neural activity distinguishes subgroups of schizophrenia patients. Biological Psychiatry, 56(12), 931937. doi:10.1016/j.biopsych.2004.09.013.CrossRefGoogle ScholarPubMed
Malaspina, D., Storer, S., Furman, V., Esser, P., Printz, D., Berman, A., … Van Heertum, R. (1999). SPECT study of visual fixation in schizophrenia and comparison subjects. Biological Psychiatry, 46(1), 8993. doi:10.1016/s0006-3223(98)00306-0.CrossRefGoogle ScholarPubMed
Mamah, D., Harms, M. P., Barch, D., Styner, M., Lieberman, J. A., & Wang, L. (2012). Hippocampal shape and volume changes with antipsychotics in early stage psychotic illness. Frontiers in Psychiatry, 3, 96. doi:10.3389/fpsyt.2012.00096.CrossRefGoogle ScholarPubMed
McDiarmid, T. A., Bernardos, A. C., & Rankin, C. H. (2017). Habituation is altered in neuropsychiatric disorders – A comprehensive review with recommendations for experimental design and analysis. Neuroscience and Biobehavioral Reviews, 80, 286305. doi:10.1016/j.neubiorev.2017.05.028.CrossRefGoogle ScholarPubMed
McHugo, M., Talati, P., Armstrong, K., Vandekar, S. N., Blackford, J. U., Woodward, N. D., & Heckers, S. (2019). Hyperactivity and reduced activation of anterior hippocampus in early psychosis. The American Journal of Psychiatry, 176(12), 10301038. doi:10.1176/appi.ajp.2019.19020151.CrossRefGoogle ScholarPubMed
McHugo, M., Talati, P., Woodward, N. D., Armstrong, K., Blackford, J. U., & Heckers, S. (2018). Regionally specific volume deficits along the hippocampal long axis in early and chronic psychosis. NeuroImage. Clinical, 20, 11061114. doi:10.1016/j.nicl.2018.10.021.CrossRefGoogle ScholarPubMed
Meister, I. G., Buelte, D., Sparing, R., & Boroojerdi, B. (2007). A repetition suppression effect lasting several days within the semantic network. Experimental Brain Research, 183(3), 371376. doi:10.1007/s00221-007-1051-8.CrossRefGoogle ScholarPubMed
Newton, R., Rouleau, A., Nylander, A.-G., Loze, J.-Y., Resemann, H. K., Steeves, S., & Crespo-Facorro, B. (2018). Diverse definitions of the early course of schizophrenia-a targeted literature review. NPJ Schizophrenia, 4(1), 21. doi:10.1038/s41537-018-0063-7.CrossRefGoogle ScholarPubMed
Niendam, T. A., Ray, K. L., Iosif, A.-M., Lesh, T. A., Ashby, S. R., Patel, P. K., … Carter, C. S. (2018). Association of age at onset and longitudinal course of prefrontal function in youth with schizophrenia. JAMA Psychiatry, 75(12), 12521260. doi:10.1001/jamapsychiatry.2018.2538.CrossRefGoogle ScholarPubMed
Olabi, B., Ellison-Wright, I., McIntosh, A. M., Wood, S. J., Bullmore, E., & Lawrie, S. M. (2011). Are there progressive brain changes in schizophrenia? A meta-analysis of structural magnetic resonance imaging studies. Biological Psychiatry, 70(1), 8896. doi:10.1016/j.biopsych.2011.01.032.CrossRefGoogle ScholarPubMed
Ongür, D., Cullen, T. J., Wolf, D. H., Rohan, M., Barreira, P., Zalesak, M., & Heckers, S. (2006). The neural basis of relational memory deficits in schizophrenia. Archives of General Psychiatry, 63(4), 356365. doi:10.1001/archpsyc.63.4.356.CrossRefGoogle ScholarPubMed
Perkins, D. O., Leserman, J., Jarskog, L. F., Graham, K., Kazmer, J., & Lieberman, J. A. (2000). Characterizing and dating the onset of symptoms in psychotic illness: The symptom onset in schizophrenia (SOS) inventory. Schizophrenia Research, 44(1), 110. doi:10.1016/s0920-9964(99)00161-9.CrossRefGoogle ScholarPubMed
Poppenk, J., Evensmoen, H. R., Moscovitch, M., & Nadel, L. (2013). Long-axis specialization of the human hippocampus. Trends in Cognitive Sciences, 17(5), 230240. doi:10.1016/j.tics.2013.03.005.CrossRefGoogle ScholarPubMed
Poppenk, J., McIntosh, A. R., & Moscovitch, M. (2016). fMRI evidence of equivalent neural suppression by repetition and prior knowledge. Neuropsychologia, 90, 159169. doi:10.1016/j.neuropsychologia.2016.06.034.CrossRefGoogle ScholarPubMed
Provenzano, F. A., Guo, J., Wall, M. M., Feng, X., Sigmon, H. C., Brucato, G., … Small, S. A. (2020). Hippocampal pathology in clinical high-risk patients and the onset of schizophrenia. Biological Psychiatry, 87(3), 234242. doi:10.1016/j.biopsych.2019.09.022.CrossRefGoogle ScholarPubMed
Purdon, S. (2005). The screen for cognitive impairment in psychiatry (SCIP): Administration manual and normative data. Edmonton, Alberta: PNL Inc.Google Scholar
Raemaekers, M., Vink, M., Zandbelt, B., van Wezel, R. J. A., Kahn, R. S., & Ramsey, N. F. (2007). Test-retest reliability of fMRI activation during prosaccades and antisaccades. NeuroImage, 36(3), 532542. doi:10.1016/j.neuroimage.2007.03.061.CrossRefGoogle ScholarPubMed
Ragland, J. D., Layher, E., Hannula, D. E., Niendam, T. A., Lesh, T. A., Solomon, M., … Ranganath, C. (2017). Impact of schizophrenia on anterior and posterior hippocampus during memory for complex scenes. NeuroImage. Clinical, 13, 8288. doi:10.1016/j.nicl.2016.11.017.CrossRefGoogle ScholarPubMed
Ramaswami, M. (2014). Network plasticity in adaptive filtering and behavioral habituation. Neuron, 82(6), 12161229. doi:10.1016/j.neuron.2014.04.035.CrossRefGoogle ScholarPubMed
Rankin, C. H., Abrams, T., Barry, R. J., Bhatnagar, S., Clayton, D. F., Colombo, J., … Thompson, R. F. (2009). Habituation revisited: An updated and revised description of the behavioral characteristics of habituation. Neurobiology of Learning and Memory, 92(2), 135138. doi:10.1016/j.nlm.2008.09.012.CrossRefGoogle ScholarPubMed
Reske, M., Kellermann, T., Habel, U., Jon Shah, N., Backes, V., von Wilmsdorff, M., … Schneider, F. (2007). Stability of emotional dysfunctions? A long-term fMRI study in first-episode schizophrenia. Journal of Psychiatric Research, 41(11), 918927. doi:10.1016/j.jpsychires.2007.02.009.CrossRefGoogle ScholarPubMed
Scheef, L., Manka, C., Daamen, M., Kühn, K.-U., Maier, W., Schild, H. H., & Jessen, F. (2010). Resting-state perfusion in nonmedicated schizophrenic patients: A continuous arterial spin-labeling 3.0-T MR study. Radiology, 256(1), 253260. doi:10.1148/radiol.10091224.CrossRefGoogle ScholarPubMed
Schobel, S. A., Chaudhury, N. H., Khan, U. A., Paniagua, B., Styner, M. A., Asllani, I., … Small, S. A. (2013). Imaging patients with psychosis and a mouse model establishes a spreading pattern of hippocampal dysfunction and implicates glutamate as a driver. Neuron, 78(1), 8193. doi:10.1016/j.neuron.2013.02.011.CrossRefGoogle Scholar
Schobel, S. A., Lewandowski, N. M., Corcoran, C. M., Moore, H., Brown, T., Malaspina, D., & Small, S. A. (2009). Differential targeting of the CA1 subfield of the hippocampal formation by schizophrenia and related psychotic disorders. Archives of General Psychiatry, 66(9), 938946. doi:10.1001/archgenpsychiatry.2009.115.CrossRefGoogle ScholarPubMed
Smucny, J., Lesh, T. A., Zarubin, V. C., Niendam, T. A., Ragland, J. D., Tully, L. M., … Carter, C. S. (2020). One-year stability of frontoparietal cognitive control network connectivity in recent onset schizophrenia: A task-related 3 T fMRI study. Schizophrenia Bulletin, 46(5), 12491258. 10.1093/schbul/sbz122.CrossRefGoogle Scholar
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014). Functional organization of the hippocampal longitudinal axis. Nature Reviews. Neuroscience, 15(10), 655669. doi:10.1038/nrn3785.CrossRefGoogle ScholarPubMed
Talati, P., Rane, S., Kose, S., Blackford, J. U., Gore, J., Donahue, M. J., & Heckers, S. (2014). Increased hippocampal CA1 cerebral blood volume in schizophrenia. NeuroImage. Clinical, 5, 359364. doi:10.1016/j.nicl.2014.07.004.CrossRefGoogle ScholarPubMed
Talati, P., Rane, S., Skinner, J., Gore, J., & Heckers, S. (2015). Increased hippocampal blood volume and normal blood flow in schizophrenia. Psychiatry Research, 232(3), 219225. doi:10.1016/j.pscychresns.2015.03.007.CrossRefGoogle ScholarPubMed
Tamminga, C. A., Southcott, S., Sacco, C., Wagner, A. D., & Ghose, S. (2012). Glutamate dysfunction in hippocampus: Relevance of dentate gyrus and CA3 signaling. Schizophrenia Bulletin, 38(5), 927935. doi:10.1093/schbul/sbs062.CrossRefGoogle ScholarPubMed
Tamminga, C. A., Thomas, B. P., Chin, R., Mihalakos, P., Youens, K., Wagner, A. D., & Preston, A. R. (2012). Hippocampal novelty activations in schizophrenia: Disease and medication effects. Schizophrenia Research, 138(2–3), 157163. doi:10.1016/j.schres.2012.03.019.CrossRefGoogle ScholarPubMed
Wechsler, D. (2001). Wechsler test of adult reading. San Antonio, TX: Pearson.Google Scholar
Weiss, A. P., Schacter, D. L., Goff, D. C., Rauch, S. L., Alpert, N. M., Fischman, A. J., & Heckers, S. (2003). Impaired hippocampal recruitment during normal modulation of memory performance in schizophrenia. Biological Psychiatry, 53(1), 4855. doi:10.1016/s0006-3223(02)01541-x.CrossRefGoogle ScholarPubMed
Williams, L. E., Blackford, J. U., Luksik, A., Gauthier, I., & Heckers, S. (2013). Reduced habituation in patients with schizophrenia. Schizophrenia Research, 151(1–3), 124132. doi:10.1016/j.schres.2013.10.017.CrossRefGoogle ScholarPubMed
Zeidman, P., & Maguire, E. A. (2016). Anterior hippocampus: The anatomy of perception, imagination and episodic memory. Nature Reviews. Neuroscience, 17(3), 173182. doi:10.1038/nrn.2015.24.CrossRefGoogle ScholarPubMed
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