Perceptual training strongly improves visual motion perception in schizophrenia
Highlights
► Visual motion processing is deficient in schizophrenia. ► Patients received neuroplasticity-based training on direction discrimination. ► Performance in patients was improved to a greater extent than in controls. ► A robust plasticity is preserved within the visual system in schizophrenia. ► Deficient perception may be a promising target for cognitive intervention.
Introduction
Cognitive impairment is a core dysfunction in schizophrenia. Research in the past few decades has indicated that cognitive deficits extend to certain early perceptual processes (Green et al., 2009, Javitt, 2009). Given that many cognitive processes and daily behaviors rely on perceptual processing, the improvement of deficient perception represents a potential primary step in behavioral intervention for schizophrenia patients; and the emerging evidence is promising. For example, perceptual training in the auditory domain has led to improvement of verbal working memory and cognition in patients (Fisher, Holland, Merzenich, & Vinogradov, 2009). It is unclear, however, whether cognitive improvements as a result of perceptual training are mediated through improvements in basic perceptual domains. To understand the underlying mechanisms, one may need to first examine the effects of perceptual training on perceptual processing itself.
Visual motion processing is deficient in schizophrenia (Chen, 2011). Patients show poor performance discriminating the speed (Brenner et al., 2003, Chen et al., 1999; Clementz et al., 2007, Kim et al., 2006) as well as the direction of visual motion stimuli (Chen et al., 2003, Slaghuis et al., 2007, Stuve et al., 1997). Brain abnormalities in motion processing have been found at levels ranging from basic neural circuitry (Chen et al., 2008, Tadin et al., 2006) to cortical systems (Chen et al., 2008, Wang et al., 2010). At present, it is unknown whether the visual motion processing deficit in schizophrenia can be ameliorated.
In healthy people, perceptual sensitivity to visual motion can be improved through training that involves extensive exposure to motion stimuli (Ball and Sekuler, 1982, Watanabe et al., 2001). Enduring and consistent improvement in a perceptual task as a result of such training is known as perceptual learning (Gibson, 1963). Perceptual learning is often specific to the stimulus features used in training (Gilbert, Sigman, & Crist, 2001). For example, subjects who have been trained on one direction of motion show increased sensitivity to the trained, but not to other, directions of motion (Ball & Sekuler, 1982). This indicates that the perceptual learning process is primarily mediated by neuroplasticity in the early stages of perceptual systems, where encoding of the stimulus features is precisely localized (Gilbert et al., 2001, Hua et al., 2010). Neuroimaging studies have provided further evidence showing that training-induced performance improvement on a visual discrimination task is associated with increased neural activation in visual processing areas like the striate cortex (Schwartz et al., 2002, Yotsumoto et al., 2009). Single cell recording studies in monkey also indicate that the biological basis of perceptual learning is linked to neuroplasticity in the sensory cortex (e.g., Zohary, Celebrini, Britten, & Newsome, 1994).
While the primary perceptual learning mechanisms are specific to the trained domain, non-specific perceptual learning mechanisms may also be at work (Fine & Jacobs, 2002). Perceptual learning seems to be able to transfer from a trained domain (e.g. one direction of motion) to an untrained parallel domain (e.g. another direction of motion) when the task for learning is easy (Liu & Weinshall, 2000) and can also generalize from complex tasks to simpler ones (Fahle, 2005, Green and Bavelier, 2003). In terms of interventions in schizophrenia, the ability of training effects to generalize would mean that bottom-up perceptual learning may potentially produce benefits for other untrained behavioral functions.
In general, improvement in perceptual sensitivity via training requires neuroplasticity mechanisms to be at work (Gilbert et al., 2001). While it is unknown at this point whether and how the mechanisms involved in perceptual learning are affected in schizophrenia, a recent hypothesis posits that neuroplasticity and synaptic functions are altered in this mental disorder (Frankle, Lerma, & Laruelle, 2003). Several lines of research seem to be consistent with this hypothesis, including genetic (Balu & Coyle, 2011), molecular (Buckley et al., 2011, Goto et al., 2010) and behavioral studies (Daskalakis, Christensen, Fitzgerald, & Chen, 2008). On the other hand, studies of cortical activations in patients showed intact or even excessive plasticity when cognitive training paradigms were applied (Edwards et al., 2010, Haut et al., 2010). Similarly, hippocampal volumetric changes in response to exercise, another indicator of neuroplasticity, appear to be normal or even more robust in schizophrenia (Pajonk et al., 2010).
In visual domains, it remains unknown whether the neuroplasticity is impaired in schizophrenia. Given that many cognitive functions rely on visual inputs, it is critical to ascertain whether or not visual plasticity can allow the improvement of abnormal visual processing through perceptual training in this mental disorder. The goal of the present study was to explore the feasibility of improving deficient visual motion perception in schizophrenia using a perceptual learning procedure. Based on robust perceptual learning effects in healthy people, and a mixed set of results regarding neuroplasticity in patients, we hypothesized that patients would show significant perceptual improvement, but to a lesser extent than controls.
Section snippets
Subjects
Seventeen patients with schizophrenia or schizoaffective disorder and 10 healthy controls participated. General inclusion criteria for both groups of participants were: age between 18 and 65, no drug or alcohol abuse in the six months prior to participation, no neurological problems such as seizure, stroke or major head injury, and IQ > 70.
Patients were recruited from McLean Hospital as well as the Greater Boston area. They were diagnosed using the Structure Clinical Interview for DSM Disorders,
Direction discrimination: the trained task
The training on direction discrimination significantly improved the performance on that task (Fig. 3a). A two-way ANOVA2 (group × training session) showed a significant main effect for training session, F(5, 120) = 7.02, p < 0.001, η2 = 0.23, but not for group, F(5, 24) = 2.45, p = 0.13, η2 = 0.09. There was a non-significant interaction effect between group and training session, F(5, 120) = 2.57, p = 0.07, η2 = 0.10.
Discussion
Schizophrenia patients showed significant performance improvement as a result of the perceptual training, as indicated by lowered perceptual thresholds in direction discrimination task after training. Counter to our original hypothesis, the extent of the perceptual improvement in the patient group was greater, not lesser, than that in the control group.
Conclusion
In the present study, patients’ performance in judging the direction of motion improved to such an extent that, after learning, they scored similarly to healthy controls prior to learning. The large training-induced change in patients’ performance suggests the presence of a significant amount of plasticity at the visual processing level. Such intrinsic properties of the visual system can be potential bases for the development of bottom-up behavioral interventions in this mental disorder.
Acknowledgments
This work was supported in part by NIH Grant MH R01 61824 and a Grant from Harvard University, both to Dr. Chen. We thank the subjects for their extensive participation, as well as Drs. Charles Stromeyer III and Tim Brown, Andrea Cataldo, Stephanie Dibble, Allyson Hodgkins, Grace Masters, Daniel Seichepine and Jenna Glasenberg for their assistance on this project.
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Present address: Harvard School of Public Health, United States.