Neural synchrony indexes disordered perception and cognition in schizophrenia

Abstract

Current views of schizophrenia suggest that it results from abnormalities in neural circuitry, but empirical evidence in the millisecond range of neural activity has been difficult to obtain. In pursuit of relevant evidence, we previously demonstrated that schizophrenia is associated with abnormal patterns of stimulus-evoked phaselocking of the electroencephalogram in the ␥ band (30 -100 Hz). These patterns may reflect impairments in neural assemblies, which have been proposed to use ␥-band oscillations as a mechanism for synchronization. Here, we report the unique finding that, in both healthy controls and schizophrenia patients, visual Gestalt stimuli elicit a ␥-band oscillation that is phase-locked to reaction time and hence may reflect processes leading to conscious perception of the stimuli. However, the frequency of this oscillation is lower in schizophrenics than in healthy individuals. This finding suggests that, although synchronization must occur for perception of the Gestalt, it occurs at a lower frequency because of a reduced capability of neural networks to support high-frequency synchronization in the brain of schizophrenics. Furthermore, the degree of phase locking of this oscillation is correlated with visual hallucinations, thought disorder, and disorganization in the schizophrenia patients. These data provide support for linking dysfunctional neural circuitry and the core symptoms of schizophrenia.electroencephalogram ͉ ␥ band C ontemporary views of schizophrenia propose that the basis of this disorder lies in the dysfunction of neural microcircuits, rather than specific brain areas or neurotransmitter systems. These views are based on postmortem studies of the brains of schizophrenia patients (SZ), which have reported abnormalities at the cellular level, including inhibitory interneurons (1-3). Moreover, animal studies suggest that such disturbances may involve the hypofunctioning of N-methyl-D-aspartate receptors on inhibitory interneurons because psychotomimetics selectively block this receptor (4, 5). Inhibitory interneurons appear to be crucial elements in the generation of synchronous neural activity in the ␤ (13-30 Hz) and ␥ (30-100 Hz) bands of the electroencephalogram (EEG) (6, 7). Evidence is accumulating that such synchronous oscillations may underlie cognitive functions such as object perception, selective attention, and working memory (8, 9), as well as consciousness (10). Thus, the analysis of high-frequency EEG oscillatory activity may provide functional evidence for neural circuitry abnormalities in schizophrenia.In earlier studies we have found that SZ exhibit deficits in ␥-band neural synchrony as measured by EEG phase locking during auditory steady-state stimulation (11) and during the perception of visual Gestalt patterns (12). In the latter study, SZ displayed several abnormalities in the early visual ␥-band oscillation in comparison with matched healthy control subjects. The most striking finding was that Gestalt stimuli failed to elicit the occipital component of the earl...

Anticipation of natural stimuli modulates EEG dynamics: physiology and simulation

“…Busch et al 2004Busch et al , 2006bTallon-Baudry et al 1996;Spencer et al 2004), the current data did not contain any systematic responses at frequencies above 30 Hz.…”

Gamma Oscillatory Power is Impaired During Cognitive Control Independent of Medication Status in First-Episode Schizophrenia

“…Gamma oscillatory deficits have been observed in schizophrenia under a wide range of experimental conditions, including in the resting state (Yeragani et al, 2006), elicited by TMS (Ferrarelli et al, 2008), with relatively simple perceptual task demands (Spencer et al, 2003;Spencer et al, 2004;Spencer et al, 2008a), in relation to motor responses (Ford et al, 2008), and with more complex cognitive demands (Cho et al, 2006), including this study. Taken together, these findings suggest that cortical oscillatory dysfunction may be a general feature of this illness.…”

“…Gamma activity has also been studied in schizophrenia using tasks with more complex processing demands. These studies have found schizophrenia patients to exhibit relatively lower frequency (Spencer et al, 2004) and decreased synchrony (Spencer et al, 2003) of an oscillation that is phase-locked to motor response in a Gestalt perception task, although others have found preserved gamma power in a different Gestalt perception task (Uhlhaas et al, 2006). Task demands with a stronger PFC-dependence have also revealed gamma deficits in schizophrenia patients, including impaired frontal gamma power (measured by magnetoencephalography) during mental arithmetic performance (Kissler et al, 2000) and an inability to mount increased delay-period gamma power in response to increasing working memory load during the N-Back (Basar-Eroglu et al, 2007).…”

Deep Brain Stimulation in Schizophrenia

“…Moreover, an association of neural oscillations with symptom dimensions has been demonstrated. Deficits in beta/gamma bands may contribute to perceptual impairments, and neural synchronization has been found correlated with positive and negative symptom dimensions of schizophrenia (Spencer et al, 2004;Uhlhaas et al, 2008;Uhlhaas et al, 2006). Changes in alpha synchronization during a memory task have been found to be correlated with task performance (Haenschel et al, 2010).…”

“…Some investigations have found correlations of neural synchronization with memory performance and sensory processing, respectively (Spencer et al, 2004;Uhlhaas et al, 2008;Uhlhaas et al, 2006;Haenschel et al, 2010). Reduced synchronization, for instance, has been demonstrated in the anterior cingulate cortex (ACC) during an auditory discrimination task (Gallinat et al, 2002).…”