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Hippocampal Plasticity in Response to Exercise in Schizophrenia

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Hippocampal Plasticity in Response to Exercise in Schizophrenia ORIGINAL ARTICLE Hippocampal Plasticity in Response to Exercise in Schizophrenia Frank-Gerald Pajonk, MD; Thomas Wobrock, MD; Oliver Gruber, MD; Harald Scherk, MD; Dorothea Berner, MD; Inge Kaizl, MD; Astrid Kierer, cand.med; Stephanie Müller, cand.med; Martin Oest, MD; Tim Meyer, MD; Martin Backens, MD; Thomas Schneider-Axmann, PhD; Allen E. Thornton, PhD; William G. Honer, MD; Peter Falkai, MD Context: Hippocampal volume is lower than expected (Rey Auditory Verbal Learning Test, Corsi block- in patients with schizophrenia; however, whether this rep- tapping test), and clinical (Positive and Negative Syn- resents a fixed deficit is uncertain. Exercise is a stimu- drome Scale) features. lus to hippocampal plasticity. Results: Following exercise training, relative hippocam- Objective: To determine whether hippocampal vol- pal volume increased significantly in patients (12%) and ume would increase with exercise in humans and whether healthy subjects (16%), with no change in the nonexer- this effect would be related to improved aerobic fitness. cise group of patients (−1%). Changes in hippocampal volume in the exercise group were correlated with im- Design: Randomized controlled study. provements in aerobic fitness measured by change in maximum oxygen consumption (r=0.71; P=.003). In the Setting: Patients attending a day hospital program or schizophrenia exercise group (but not the controls), an outpatient clinic. change in hippocampal volume was associated with a 35% increase in the N-acetylaspartate to creatine ratio in the Patients or Other Participants: Male patients with hippocampus. Finally, improvement in test scores for chronic schizophrenia and matched healthy subjects. short-term memory in the combined exercise and non- exercise schizophrenia group was correlated with change Interventions: Aerobic exercise training (cycling) and in hippocampal volume (r=0.51; PϽ.05). playing table football (control group) for a period of 3 months. Conclusion: These results indicate that in both healthy subjects and patients with schizophrenia hippocampal Main Outcome Measures: Magnetic resonance imaging volume is plastic in response to aerobic exercise. of the hippocampus. Secondary outcome measures were magnetic resonance spectroscopy, neuropsychological Arch Gen Psychiatry. 2010;67(2):133-143 CHIZOPHRENIA CAN BE CONSID- in healthy humans can be stimulated by ered as an illness beginning in exercise.5 young adults, but related to a In healthy humans, aerobic exercise re- predisposition in brain devel- sulted in increased hippocampal blood vol- opment. In contrast to other ume, which correlated with improve- Sillnesses that may display psychotic fea- ment in capacity for aerobic exercise.5 In tures, such as bipolar disorder, schizophre- a parallel study of healthy mice, exercise nia is often characterized by incomplete re- also resulted in increased hippocampal covery of psychotic symptoms and persistent blood volume, which was correlated with disability.1 These clinical features of ill- increased neurogenesis. Other studies also ness may relate to an impairment of neural indicate increased cardiovascular fitness plasticity or mechanisms of reorganizing in humans to be associated with greater brain function in response to a challenge.2 activation of cortical networks during cog- Adult neurogenesis is one component of nitive challenges.6 Although the effects of plasticity. Abnormalities of olfactory neu- exercise on hippocampal volume in hu- rons and of hippocampal granule cell neu- mans are unknown, several studies indi- rons in schizophrenia indicate that impair- cate plasticity of gray matter volume in hu- ment in adult neurogenesis could contribute mans to be associated with learning and to dysfunction of neural plasticity in schizo- other types of training.7-9 phrenia.3,4 Stimuli to modify olfactory neu- Aerobic exercise may be an informa- Author Affiliations are listed at rogenesis in humans are unclear. How- tive probe into the capacity of the hippo- the end of this article. ever, adult neurogenesis in the hippocampus campus for plasticity in schizophrenia. (REPRINTED) ARCH GEN PSYCHIATRY/ VOL 67 (NO. 2), FEB 2010 WWW.ARCHGENPSYCHIATRY.COM 133 ©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/23/2021 Table 1. Demographic Values for Subjects Participating in the Study Mean (SD) Schizophrenia Schizophrenia Control Group Exercise Group Nonexercise Group (n=8) (n=8) (n=8) Age, y 34.8 (10.2) 32.9 (10.6) 37.4 (8.1) Education, y 11.0 (1.7) 9.8 (1.4) 10.3 (2.4) Vocabulary test IQ 103.6 (6.4) 102.4 (12.3) 106.8 (20.6) Duration of illness, y 8.4 (8.4) 12.5 (4.5) Antipsychotic medication dose, defined daily doses, CPZ 733 (321) 769 (503) Antipsychotic medication, No. Clozapine 55 Olanzapine 1 Amisulpride 2 Risperidone 33 Haloperidol 11 Quetiapine fumarate 1 Fluphenazine 1 Sulpiride 1 Promethazine 1 Flupenthixol 1 Zotepine 1 Antidepressant medication, No. Trimipramine for sleep 1 Mirtazapine 1 Venlafaxine hydrochloride 2 Paroxetine hydrochloride 1 Amitriptyline hydrochloride 1 PANSS score Total 68.1 (17.6) 65.9 (13.9) Positive 13.6 (3.4) 13.5 (3.5) Negative 22.1 (5.7) 22.0 (7.8) CGI score 5.1 (1.0) 4.9 (1.0) Abbreviations: CGI, Clinical Global Impression scale; CPZ, chlorpromazine equivalent dose; PANSS, Positive and Negative Syndrome Scale. Smaller volume of the hippocampus is a well-replicated METHODS feature of schizophrenia and appears related to neuro- 10,11 nal atrophy and loss of neuropil. However, whether SUBJECTS hippocampal volume in schizophrenia is static or becomes progressively smaller during the course of ill- Approximately two-thirds of patients with schizophrenia ness remains uncertain.10,12,13 Antipsychotic drug treat- approached to participate in the study agreed and provided ment does not appear to correct the low hippocampal written informed consent. The randomization strategy was volume in schizophrenia, although there are few longi- designed by an independent statistician. Subjects with schizo- tudinal studies.13-15 There is some indication that phrenia were recruited and randomized in blocks of 2 to 4 to changes in medication associated with increases of hip- an exercise group or a nonexercise group. This strategy was pocampal volume over time in schizophrenia are linked adopted to increase the motivation for adherence to the exer- with some improvement in symptoms.16 While the cise intervention through participation as a small group, and pairs of subjects were required for the nonexercise (table foot- mechanism remains unclear, these findings suggest a ball) intervention. The person doing the recruitment (T.W.) degree of preserved plasticity in the hippocampus in was unaware of the sequence of assignments, and the person schizophrenia. doing the assignments (F.P.) was unaware of the clinical sta- The present study was designed to test a primary hy- tus of the participants. Recruitment and randomization con- pothesis that hippocampal volume would increase with tinued until 8 subjects in each group completed the 3-month exercise in healthy control subjects as well as in pa- period of study. We then screened healthy control subjects, tients with schizophrenia. We sought to determine if the with the goal of recruiting a comparison exercise group that hypothesized increase in hippocampal volume in schizo- would have similar demographics (Table 1)(Figure 1)as well as verbal intelligence, body mass index, and weight- phrenia was related to exercise rather than nonspecific ˙ effects of participating in research. As secondary objec- adjusted peak oxygen uptake (VO2) as the schizophrenia exer- cise group. Sample size was estimated from previous studies tives, we hypothesized that exercise-induced change in of small groups of subjects with schizophrenia where changes hippocampal volume in schizophrenia might be associ- in subcortical structure volumes were demonstrated after ated with clinical or cognitive improvement and with an switching from typical to atypical antipsychotic drug increase of N-acetylaspartate (NAA), a neuronal marker therapy.17,18 The study was carried out from June 2005 to Sep- in magnetic resonance spectroscopy (MRS). tember 2006. (REPRINTED) ARCH GEN PSYCHIATRY/ VOL 67 (NO. 2), FEB 2010 WWW.ARCHGENPSYCHIATRY.COM 134 ©2010 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/23/2021 37 Patients screened 122 Controls screened 114 (93%) Excluded 13 (35%) Excluded (declined) (demographic mismatch) 24 (65%) Randomized 8 (7%) Matched controls 11 Allocated to table football 13 Allocated to aerobic exercise 8 Allocated to aerobic exercise 11 Received intervention 13 Received intervention 8 Received intervention 8 (73%) Completed study 8 (62%) Completed study 3 (27%) Discontinued 5 (38%) Discontinued 8 (100%) Completed study 2 (18%) Protocol violation 3 (23%) Protocol violation 0 (0%) Discontinued 1 (9%) Withdrew consent 2 (15%) Withdrew consent 8 Included in analysis 8 Included in analysis 8 Included in analysis 3 Excluded because of discontinuation 5 Excluded because of discontinuation 0 Excluded Figure 1. Flow diagram for the study. Subjects ranged from 20 to 51 years of age (mean [SD], 35.0 the expectation to reach a total exercise duration of at least 10 [9.5] years), and there was no difference in mean age between minutes. This protocol was held constant on an intraindividual groups. Subjects with schizophrenia were diagnosed accord- basis during all tests of the study. A 6-lead electrocardiogram was
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