Skip to content

Advertisement

  • Research article
  • Open Access
  • Open Peer Review

Impact of childhood trauma on sensory gating in patients with first-episode schizophrenia

  • 1,
  • 1,
  • 1,
  • 1,
  • 1,
  • 2,
  • 1 and
  • 1Email author
BMC Psychiatry201818:258

https://doi.org/10.1186/s12888-018-1807-7

  • Received: 13 August 2017
  • Accepted: 5 July 2018
  • Published:
Open Peer Review reports

Abstract

Background

Childhood trauma (CT) has been found to contribute to the onset of schizophrenia and auditory sensory gating deficit is a leading endophenotype for schizophrenia. However, the association between the CT and sensory gating in first-episode schizophrenia remains elusive.

Methods

Fifty-six patients and 49 age and sex-matched healthy controls were assessed using the Childhood Trauma Questionnaire-Short Form (CTQ-SF) for CT and Positive and Negative Syndrome Scale (PANSS) for symptoms severity. Sensory gating was tested using the modified paradigm, perceived spatial separation-induced prepulse inhibition (PSS-PPI), and the perceived spatial co-location PPI (PSC-PPI or classical PPI).

Results

Comparing with healthy controls, the patients had significantly higher score on sexual abuse (t = 2.729, p < 0.05), lower PSS- PPI, % (ISI = 120 ms and ISI = 60 ms) (t = − 3.089, − 4.196, p < 0.05). Univariate analysis revealed the absence of a significant correlation among CT, PPI paradigms and symptoms. However, multiple linear regression analyses demonstrated the CTQ-SF total was negatively associated with PSS PPI (ISI = 120 ms) (p = 0.018).

Conclusion

The current study illustrates that the impact of CT on sensory gating in patients with first-episode schizophrenia, and thus we conclude that CT may be a risk factor to the occurrence of schizophrenia through its impact on sensory gating.

Keywords

  • Childhood trauma
  • Sensory gating
  • Schizophrenia

Background

Schizophrenia can be understood as a complex illness of adaptation to social context. Although heritability is often emphasized, the fact that occurrence is associated with environmental factors such as childhood trauma (CT) suggests that exposure to life stress may play an important role in developing “social” brain during sensitive periods [1]. Childhood adversities, particularly exposure to multiple adversities involving hostility, threat, and CT (emotional, physical, and sexual abuse; emotional and physical neglect) have been found to contribute to the onset of psychiatric disorder including schizophrenia [24].

Auditory sensory gating deficit is a leading endophenotype for schizophrenia [5]. The prepulse inhibition (PPI) is the weakening of acoustic startle reflex (ASR) when a weaker sensory stimulus precedes the startling stimulus [6], which is considered as a good indicator of sensory gating [7]. PPI impairment has been found to always be associated with core features of schizophrenia, such as aggressive behavior [8] and positive symptoms [9, 10], and relatively stable across treatment conditions [11]. It is also considered as an early sign or residual symptom of schizophrenia [12, 13].

The social isolation rat model shares some similarities with the humans experiencing CT and some neurobiological changes in socially isolated rats can mimic characteristics of schizophrenia, therefore it can serve as a model of schizophrenia [14]. Studies show that socially isolated rats exhibit increased level of ASR and produce specific deficits in PPI [6, 15]. Furthermore, exposure to CT during puberty was associated with increased risk for neuropsychiatric disorders through PPI deficit in rats [16].

In the previously study, we found sexual abuse can be a predisposing factor that affects sensorimotor gating in the patients with chronic schizophrenia [17]. To date, the association between the ASR, PPI and CT in first-episode schizophrenia has not been explored. Therefore, we aimed to examine the relationship between CT, ASR and PPI in Chinese patients diagnosed with first-episode schizophrenia in the current study.

Methods

Subjects

All participants were inpatients or outpatients of Beijing Anding Hospital, Capital Medical University in Beijing, China. The inclusion criteria were: (1) Met the diagnostic criteria of first-episode (less than 60 months) schizophrenia based on the Structured Clinical Interview for DSM-IV (SCID) [18]; (2) Had been clinically stable for > 12 weeks; (3) had a IQ above 80 on the Wechsler Adult Intelligence Scale (CWAIS) [19] and were able to read, comprehend and sign the consent. Patients were excluded if they were clinically unstable. In addition, 49 individuals without severe mental disorders or current substance use (included nicotine abuse) were recruited from the same geographical areas to serve as healthy controls for the PPI test battery and CTQ assessment (Controls’ age mean ± SD: 26.2 ± 3.9; years of education mean ± SD:14.0 ± 2.3).

The protocol of this study was revised and approved by the ethics committee of Beijing Anding Hospital, Beijing, China. We followed the Declaration of Helsinki while we conducting the research. Each patient signed an informed written consent, an overseeing mental health expert have ruled that all adult patients and participants have been capable of ethically and medically consenting for their participation in the research.

In the case of members of this study may not be capable of providing ethical consent for their participation, we would provide a legal guardian or representative to provide consent to participate in their stead. A total of 62 eligible patients between the age of 16 and 65 years old were initially enrolled, however, 10 patients (10.7%) dropped out from the study.

Assessment of childhood trauma questionnaire – Short form (CTQ-SF)

We used the CTQ-SF to screen for CT in our patient and the healthy controls. The CTQ-SF is a 28-item retrospective self-report survey of CT experiences, which has five categories for children 12 years and older [20]. The five subscales included were emotional abuse (EA), physical abuse (PA), sexual abuse (SA), emotional neglect (EN) and physical neglect (PN). Each subscale contains five items [21]. The Chinese version of CTQ-SF has been shown to have good validity and reliability [22].

Assessment of psychiatric symptomatology and demographic features

We used the Positive and Negative Symptoms Scale (PANSS) to evaluate the symptom of the patients [23]. Furthermore, we used locally-developed data collection tables to collect demographic characteristics (age at onset, age of first treatment seeking, the duration of untreated psychosis).

Assessment of startle reflex

Apparatus

The experiments was conducted in a sound shielded room, and the temperature and humidity was comfortable. Two Ag/AgCl electrodes (diameter, 0.4 cm; resistance <5kΩ) were positioned on below and lateral to the right eye, over the orbicularis oculi muscle. Acoustic startle reflection was measured as the eyeblink component from EMG activity (filtering, 100–1000 Hz; amplifying, 10,000). Acoustic signals were delivered binaurally through Sennheiser HD 600 headphone. Acoustic sound intensity were calibrated by AUDit and System 824 audiometer calibration (Larson Davis, USA).

Testing procedure

A new designed paradigm was used in PPI testing. The prepulse sound (acoustic intensity, 65 dB SPL; duration, 150 ms; broadband white noise) was performed from headphones with interaural leading time differences at each ear onset delay 3 ms (left ear leading or right ear leading). Moreover, the background noise (acoustic intensity 60 dB SPL from 0 to 10 kHz) was presented in this testing as a masker (interaural leading time differences, 3 ms), and the background noise was contributed to a fused noise-masker signal between prepulse sound (target sound) and the background noise (masker). As a result of precedence effect, two types of perceived spatial relationships were generated: perceptual spatial separation PPI (PSS PPI) and perceptual spatial co-location PPI (PSC PPI). A trial performed a prepulse stimuli, followed by a startling pulse stimuli of 104 dB SPL broadband white nosie for 40 ms. Two lead inter-stimulus interval (ISI) (prepulse onset to pulse onset) were used (60 ms, 120 ms). Then a new trial started in a random time (15 to 25 s). Thus, four trial combinations (PSC PPI or PSS PPI * ISI 120 ms or 60 m’s) were performed in the experiment. We described the detailed measurement procedures in our other published articles (Fig. 1) [24].
Fig. 1
Fig. 1

Schematic illustration of the prepulse inhibition paradigm. In a block design (7 min), a background wideband noise was continuously delivered as the masker (left leading or right leading), 7 trials contained the startling (pulse) sound alone, and 20 trials contained the prepulse (left leading or right leading) 120 ms or 60 ms preceding the startling (pulse) noise. Trials in each block were presented randomly with the inter-trial interval about 20 s. Note: RNRP (RNLP): right leading masking with prepulse co-location (separation); LNLP (LNRP): left leading masking with prepulse co-location (separation). We have published this paradigm in our privous paper ([24])

Statistical analysis

We used student’s t-test to compare the startle activity, PPI and CT in patients and healthy controls. Spearman’s correlation was used to evaluate the correlation among symptoms, PPI and CT. In addition, a multiple linear regression analysis was conducted to investigate the association between childhood trauma and PPI. We used the Statistical Package of Social Sciences (SPSS, version 16.0) to conduct the statistical analyses.

Results

Demographics features and CT

This study included 56 patients with first-episode schizophrenia (22 males and 34 females) with an average age 25.9 ± 6.8 years (). The duration of untreated psychosis was 20.33 ± 18.14 months (1 to 60). Forty-nine healthy controls were recruited from the same geographical areas. The patients had higher score of SA than health controls (actual scores 6.47 vs 5.50, t = 2.729, p < 0.05). The patients had lower PSS PPI (both ISI = 120 ms, ISI = 60 ms) than healthy controls (t = − 3.089, − 4.196, p < 0.05, respectively). Demographic data and clinical features of the enrolled patients are summarized in Table 1.
Table 1

Demographic and clinical characteristics of schizophrenia patients and controls

 

Schizophrenia patients (N = 56)

Controls (N = 49)

X2/t

P

Gender, M/F

22/34

25/24

1.442

0.245

Age, years

25.90 ± 6.80

26.21 ± 3.90

− 0.274

0.785

Education, years

13.18 ± 3.24

14.12 ± 3.27

−1.372

0.173

DUP, months

29.92 ± 29.63

Drug-naïve/ on medication

24/32

Risperidone 10

Paliperidone 6

Olanzapine 7

Aripiprazole 6

Quetiapine 3

On medication>2w/<2w

11/21

PANSS

 Total

82.28 + 22.32

 Positive

22.57 ± 7.17

 Negative

19.25 ± 9.33

 General Psychopathology

43.02 ± 5.57

Childhood trauma

 Total

42.89 ± 11.60

38.60 ± 8.86

1.919

0.058

 Emotional abuse

7.97 ± 3.22

7.00 ± 2.48

1.589

0.116

 Physical abuse

6.11 ± 2.15

6.26 ± 2.08

− 0.314

0.754

 Sexual abuse

6.47 ± 2.13

5.50 ± 1.06

2.729

0.008

 Emotional neglect

12.83 ± 5.04

10.97 ± 3.94

1.910

0.060

 Physical neglect

9.87 ± 3.16

8.86 ± 2.31

1.679

0.097

PPI index

 Startle

77.41 ± 36.82

74.73 ± 30.33

0.322

0.748

 PPI (ISI = 120 ms), %

  PSC PPI

20.20 ± 25.86

27.77 ± 20.31

−1.321

0.191

  PSS PPI

21.06 ± 23.13

37.82 ± 20.58

−3.089

0.003

 PPI (ISI = 60 ms), %

  PSC PPI

19.98 ± 19.60

28.45 ± 18.57

−1.748

0.086

  PSS PPI

21.03 ± 17.66

41.07 ± 19.56

−4.196

0.000

DUP duration of untreatment psychosis, PANSS Positive and Negative Syndrome Scale, PSC PPI perceived spatial co-location PPI, PSS PPI perceived spatial separation

Correlations among CT, sensory gating and symptoms

There were no significant correlation among CT, PPI and symptoms after the multiple comparison correction (Table 2). Furthermore, we did not observe significant associations between CT and PPI after the multiple comparison correction (Table 3).
Table 2

The relationship among childhood trauma, PPI, and symptoms of schizophrenia

 

Positive

Negative

General Psychopathology

PANSS Total

Childhood trauma

 Emotional abuse

0.002

0.060

−0.126

−0.038

 Physical abuse

0.317

0.143

0.186

0.312

 Sexual abuse

−0.038

0.198

0.124

0.149

 Emotional neglect

0.456 (0.005)

0.075

−0.259

0.131

 Physical neglect

0.284

0.399 (0.018)

0.071

0.455 (0.008)

 Total score

0.366 (0.036)

0.185

−0.132

0.220

PPI index

 Startle

−0.113

−0.340

− 0.011

−0.210

 PSC PPI120

−0.373

−0.185

− 0.131

−0.240

 PSS PPI120

−0.466 (0.004)

−0.231

− 0.302

−0.403

 PSC PPI60

−0.216

−0.191

− 0.136

−0.223

 PSS PPI60

−0.290

−0.322

− 0.207

−0.369

PSC PPI perceived spatial co-location PPI, PSS PPI perceived spatial separation, PPI prepulse inhibition

Table 3

The relationship between the specific of CT and PPI in first-episode schizophrenia

 

Startle

PSC PPI120

PSS PPI120

PSC PPI60

PSS PPI60

Emotional abuse

0.194

−0.268

− 0.139

−0.591 (0.006)

−0.236

Physical abuse

−0.119

0.024

−0.507 (0.019)

−0.146

− 0.206

Sexual abuse

−0.036

0.021

−0.289

− 0.239

−0.354

Emotional neglect

−0.287

−0.064

− 0.203

−0.370

− 0.193

Physical neglect

0.016

−0.053

−0.258

− 0.338

−0.371

Total score

−0.112

−0.095

− 0.378

−0.495 (0.026)

− 0.394

PSC PPI perceived spatial co-location PPI, PSS PPI perceived spatial separation PPI, CT childhood trauma, PPI prepulse inhibition

Regression analyses for CT subtypes, demographic features and PSS PPI

The multiple linear regression analyses showed that total score of CTQ-SF was negatively correlated with PSS PPI (ISI = 120 ms) (p = 0.018) (Table 4). We did not identify any type of trauma significantly correlated with either PSC PPI or PSS PPI (ISI = 60 ms) (data not shown).
Table 4

Multiple linear regression analyzing the impact of demographics, childhood trauma on PSS PPI (ISI = 120 ms)

PPI subscale

Odds ratio

95% CI

p

PSS PPI

 Constant

71.108

3.660~ 70.814

0.011

  Childhood trauma

−1.542

−2.775~ − 0.309

0.018

  DUP

0.431

0.021~ 0.840

0.041

R2 = 0.531, Adjusted R2 = 0.452, F = 6.784, P = 0.011

DUP the duration of untreatment psychosis, Dependent variables: continuous and normally distributed: Independent variables: Categorical variable: sex: 1. male 2. female; Smoke history: 1.No 2.Yes; the rest of variable are continuous: age, dup, education years; PSS PPI perceived spatial separation prepulse inhibition;

Discussion

We examined the effect of CT on PPI in patients with first-episode schizophrenia (course of illness was less than 60 months). Overall, the patients had significantly higher score on SA and had more PPI deficit than healthy controls. More importantly, we found that CT was negatively correlated with PPI in the regression analysis.

CT has been demonstrated to have an impact on adult mental health, and exposure to early trauma has been linked to many psychopathologies, including schizophrenia [4]. In the current study, we found that patients with first-episode schizophrenia experienced higher level of SA. A number of studies in a range of samples attest to a link between childhood SA and psychosis, and SA before the age of 16 was strongly associated with schizophrenia, particularly if it involved non-consensual sexual intercourse [25]. A possible mechanism may be demonstrated via a neurodevelopmental model. Effects of SA on neurodevelopmental growth of the individual may give rise to neurocognitive deficits, further leading to the occurrence of schizophrenia [26]; We also found the patients had more severe PPI deficit than healthy controls, which is consistent with findings of other studies [7, 9, 27].

In the current study, we observed a negative correlation between CTQ-SF total and PSS PPI in patients. Evidence from animal studies may shed some light on the mechanism of exposure to traumatizing experiences on startle response and psychotic symptoms. One study, based on an experimental animal model, found that early life adversity during puberty was associated with increased risk for mental illness through sensory gating deficits [16]. Other study found that social isolation tend to have effects on PPI in rats [28]. Moreover, CT was associated with increased startle response in human [29]. Our findings showed that CT was indeed associated with sensory gating in first-episode schizophrenia, which attributed to the impact of early life adversity on neurodevelopment [26].

CT in humans shares some similarities with the socially isolated rat. At the behavioral level, social isolation induces hyperlocomotion, and dysfunctions in conditioned learning, reversal learning, and memory. [30]. At the endophenotype level, social isolation induces abnormalities in startle reflex and PPI. Moreover, social isolation causes changes of neurotransmitters, such as the increase of dopamine in the nucleus accumbens, the amygdala and other brain regions in the limbic system, the decrease of dopamine in medial prefrontal cortex, the decrease of 5-HT in the nucleus accumbens and the hippocampus, and changes of glutamine in the prefrontal cortex [30]. The proposed traumagenic neurodevelopmental model of schizophrenia shares similarities between the impact of CT on the brain development and the neurological abnormalities found in schizophrenia [26]. And, PPI is an important index which can reflect sensory gating function and the neurodevelopment [7]. So, we speculated that CT in human may be the risk factors to the occurrence of schizophrenia through its effects on sensory gating, and CT could cause a gene-environment interaction that result in the expression of schizophrenic symptoms.

This study has a few limitations: (1) The current study was a case-control study, a follow up study may be needed in the future to test the effect of CT on the development of sensory gating. (2). Psychotropic drugs with sedative effect have effects on PPI. In this study, 32 patients have taken drugs, which may have some influence on the results. (3). CT is deeply associated with both child factor and parental factor (for example parents’ neurodevelopmental disorder or psychiatric disease). Furthermore, it is suggested that subjects with sub-clinical autistic traits might have impaired sensory gating from birth. Unfortunately, we have not collected the information about developmental course, thus the possibilities that schizophrenic patients might have comorbid developmental disorders (especially ASD), which lead to impaired sensory gating observed in patients group.

Conclusion

The patients with first-episode schizophrenia experienced a higher level of SA and deficit of sensory gating. Furthermore CT have effects on sensory gating, which may be contribute to the onset of schizophrenia.

Abbreviations

ASR: 

Acoustic startle reflex

CT: 

Childhood trauma

CTQ-SF: 

The Childhood Trauma Questionnaire-Short Form

CWAIS: 

The Wechsler Adult Intelligence Scale

EA: 

Emotional abuse

EN: 

Emotional neglect

ISI: 

Inter-stimulus interval

PA: 

Physical abuse

PANSS: 

Positive and Negative Syndrome Scale

PN: 

Physical neglect

PPI: 

The prepulse inhibition

PSC PPI: 

The perceived spatial co-location PPI

PSS PPI: 

Perceived spatial separation-induced repulse inhibition (PSS PPI)

SA: 

Sexual abuse

SCID: 

The Structured Clinical Interview for DSM-IV

Declarations

Acknowledgements

Thank for Medjaden Bioscience Limited edited and proofread the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (81601169, 81471365), the Beijing Municipal Administration of Hospital Youth Program (QML20161901), and Neuroscience research program of the Beijing science and technology plan (Z161100002616017) for the design and collection of the study. This work was supported by the Medicine and Clinical Cooperative Research Program of Capital Medical University (No. 16JL25), the Beijing Municipal Administration of Hospitals Clinical Medicine Development of Special Funding Support (XLMX201807), and Capital’s Funds for Health Improvement and Research (2018–2-2123) for the analysis, and interpretation of data and in writing the manuscript.

Availability of data and materials

Data are available from the first and the corresponding authors.

Authors’ contributions

CYW and XBL conceived and designed the experiments; XBL, QJB, QT, NBY and ZM performed the experiments; XBL, QT and QJB analyzed the results and performed statistical analysis; YJW and WZ acquired the reagents/materials and data analysis. Finally, XBL, QJB written (original draft preparation) and, CYW written (review and editing). All authors read and approved the final manuscript.

Ethics approval and consent to participate

The protocol of this study was revised and approved by the ethics committee (IRB) of Beijing Anding Hospital, Beijing, China. Each patient signed an informed written consent.

Consent for publication

Not applicable.

Competing interests

The authors declare no conflicts of interest with regard to this manuscript.

Publisher’s Note

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

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
The National Clinical Research Center for Mental Disorders & Beijing Key Laboratory of Mental Disorders & Beijing Institute for Brain Disorders Center of Schizophrenia, Beijing Anding Hospital, Capital Medical University, No.5 Ankang Lane, Dewai Avenue, Xicheng District, Beijing, 100088, China
(2)
The Affiliated Brain Hospital of Guangzhou Medical University (Guangzhou Huiai Hospital), Guangzhou, China

References

  1. van Os J, Kenis G, Rutten BP. The environment and schizophrenia. Nature. 2010;468(7321):203–12.View ArticlePubMedGoogle Scholar
  2. Morgan C, Gayer-Anderson C. Childhood adversities and psychosis: evidence, challenges, implications. World Psychiatry. 2016;15(2):93–102.View ArticlePubMedPubMed CentralGoogle Scholar
  3. Owen MJ, Sawa A, Mortensen PB. Schizophrenia. Lancet. 2016;388(10039):86–97.View ArticlePubMedPubMed CentralGoogle Scholar
  4. Varese F, Smeets F, Drukker M, Lieverse R, Lataster T, Viechtbauer W, Read J, van Os J, Bentall RP. Childhood adversities increase the risk of psychosis: a meta-analysis of patient-control, prospective- and cross-sectional cohort studies. Schizophr Bull. 2012;38(4):661–71.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Hall MH, Taylor G, Salisbury DF, Levy DL. Sensory gating event-related potentials and oscillations in schizophrenia patients and their unaffected relatives. Schizophr Bull. 2011;37(6):1187–99.View ArticlePubMedGoogle Scholar
  6. Li N, Ping J, Wu R, Wang C, Wu X, Li L. Auditory fear conditioning modulates prepulse inhibition in socially reared rats and isolation-reared rats. Behav Neurosci. 2008;122(1):107–18.View ArticlePubMedGoogle Scholar
  7. Roussos P, Giakoumaki SG, Zouraraki C, Fullard JF, Karagiorga VE, Tsapakis EM, Petraki Z, Siever LJ, Lencz T, Malhotra A, et al. The relationship of common risk variants and polygenic risk for schizophrenia to sensorimotor gating. Biol Psychiatry. 2016;79(12):988–96.View ArticlePubMedGoogle Scholar
  8. Sedgwick O, Young S, Greer B, Arnold J, Parsons A, Puzzo I, Terracciano M, Das M, Kumari V. Sensorimotor gating characteristics of violent men with comorbid psychosis and dissocial personality disorder: relationship with antisocial traits and psychosocial deprivation. Schizophr Res. 2017. https://doi.org/10.1016/j.schres.2017.06.045. [Epub ahead of print]
  9. Kumari V, Fannon D, Geyer MA, Premkumar P, Antonova E, Simmons A, Kuipers E. Cortical grey matter volume and sensorimotor gating in schizophrenia. Cortex. 2008;44(9):1206–14.View ArticlePubMedPubMed CentralGoogle Scholar
  10. Wang ZR, Tan YL, Yang FD, Zhang WF, Zou YZ, Tan SP, Song CS, Li YL, Zhang WH, Zhou DF. Impaired prepulse inhibition of acoustic startle in Chinese patients with first-episode, medication-naive schizophrenia. Chin Med J. 2013;126(3):526–31.PubMedGoogle Scholar
  11. Duncan E, Szilagyi S, Schwartz M, Kunzova A, Negi S, Efferen T, Peselow E, Chakravorty S, Stephanides M, Harmon J, et al. Prepulse inhibition of acoustic startle in subjects with schizophrenia treated with olanzapine or haloperidol. Psychiatry Res. 2003;120(1):1–12.View ArticlePubMedGoogle Scholar
  12. De Koning MB, Bloemen OJ, Van Duin ED, Booij J, Abel KM, De Haan L, Linszen DH, Van Amelsvoort TA. Pre-pulse inhibition and striatal dopamine in subjects at an ultra-high risk for psychosis. J Psychopharmacol. 2014;28(6):553–60.View ArticlePubMedGoogle Scholar
  13. Parwani A, Duncan EJ, Bartlett E, Madonick SH, Efferen TR, Rajan R, Sanfilipo M, Chappell PB, Chakravorty S, Gonzenbach S, et al. Impaired prepulse inhibition of acoustic startle in schizophrenia. Biol Psychiatry. 2000;47(7):662–9.View ArticlePubMedGoogle Scholar
  14. Geyer MA, Wilkinson LS, Humby T, Robbins TW. Isolation rearing of rats produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia. Biol Psychiatry. 1993;34(6):361–72.View ArticlePubMedGoogle Scholar
  15. Wilkinson LS, Killcross SS, Humby T, Hall FS, Geyer MA, Robbins TW. Social isolation in the rat produces developmentally specific deficits in prepulse inhibition of the acoustic startle response without disrupting latent inhibition. Neuropsychopharmacology. 1994;10(1):61–72.View ArticlePubMedGoogle Scholar
  16. Giovanoli S, Engler H, Engler A, Richetto J, Voget M, Willi R, Winter C, Riva MA, Mortensen PB, Feldon J, et al. Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science. 2013;339(6123):1095–9.View ArticlePubMedGoogle Scholar
  17. Li X, Tian Q, Bo Q, Zhang G, Zheng W, Wen Y, Tang Y, Wang C. Impact of childhood trauma on sensorimotor gating in Chinese patients with chronic schizophrenia. Psychiatry Res. 2017; https://doi.org/10.1016/j.psychres.2018.1001.1037
  18. First MB, Spitzer RL, Gibbon M, Williams JB. Structured clinical interview for DSM-IVо Axis I disorders (SCID-I), Clinician Version, Administration Booklet. Arlington: American Psychiatric Pub; 2012.Google Scholar
  19. Dai XY, Gong YX. A comparative study of factor analysis: original vs revised version of Chinese version Wechsler adult intelligence scale (WAIS to WAIS-R). Psychol Bull. 1987;19:70–8.Google Scholar
  20. Bernstein DP, Stein JA, Newcomb MD, Walker E, Pogge D, Ahluvalia T, Stokes J, Handelsman L, Medrano M, Desmond D. Development and validation of a brief screening version of the childhood trauma questionnaire. Child Abuse Negl. 2003;27(2):169–90.View ArticlePubMedGoogle Scholar
  21. Bernstein DP, Fink L. Childhood trauma questionnaire: A retrospective self-report:Manual. San Antonio, TX: The Psychological Corporation; 1998.Google Scholar
  22. Zhao XF, Zhang YL, Li LF, Zhou YF, Li HZ, Yang SC. Reliability and validity of the Chinese version of childhood trauma questionnarie. Chin J Clin Rehab. 2005;9(20):105–7.Google Scholar
  23. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 1987;13(2):261–76.View ArticlePubMedGoogle Scholar
  24. Yang NB, Tian Q, Fan Y, Bo QJ, Zhang L, Li L, Wang CY. Deficits of perceived spatial separation induced prepulse inhibition in patients with schizophrenia: relationships to symptoms and neurocognition. BMC Psychiatry. 2017;17(1):135.View ArticlePubMedPubMed CentralGoogle Scholar
  25. Bebbington P, Jonas S, Kuipers E, King M, Cooper C, Brugha T, Meltzer H, McManus S, Jenkins R. Childhood sexual abuse and psychosis: data from a cross-sectional national psychiatric survey in England. Br J Psychiatry J Ment Sci. 2011;199(1):29–37.View ArticleGoogle Scholar
  26. Shannon C, Douse K, McCusker C, Feeney L, Barrett S, Mulholland C. The association between childhood trauma and memory functioning in schizophrenia. Schizophr Bull. 2011;37(3):531–7.View ArticlePubMedGoogle Scholar
  27. Ellwanger J, Geyer MA, Braff DL. The relationship of age to prepulse inhibition and habituation of the acoustic startle response. Biol Psychol. 2003;62(3):175–95.View ArticlePubMedGoogle Scholar
  28. Li L, Du Y, Li N, Wu X, Wu Y. Top-down modulation of prepulse inhibition of the startle reflex in humans and rats. Neurosci Biobehav Rev. 2009;33(8):1157–67.View ArticlePubMedGoogle Scholar
  29. Jovanovic T, Blanding NQ, Norrholm SD, Duncan E, Bradley B, Ressler KJ. Childhood abuse is associated with increased startle reactivity in adulthood. Depress Anxiety. 2009;26(11):1018–26.View ArticlePubMedPubMed CentralGoogle Scholar
  30. Lei M, Luo L, Ma S, Zhang Y, Wu Y, Li L. Behavioral and neurobiological abnormalities induced by social isolation as a useful animal model of schizophrenia. Acta Phys Sin. 2013;65(1):8.Google Scholar

Copyright

© The Author(s). 2018

Advertisement