The Neural Substrates of Impaired Prosodic Detection in Schizophrenia and Its Sensorial Antecedents

Nathan Kline Institute, Orangeburg, New York, United States
American Journal of Psychiatry (Impact Factor: 13.56). 04/2007; 164(3):474-82. DOI: 10.1176/appi.ajp.164.3.474
Source: PubMed

ABSTRACT Individuals with schizophrenia show severe deficits in their ability to decode emotions based upon vocal inflection (affective prosody). This study examined neural substrates of prosodic dysfunction in schizophrenia with voxelwise analysis of diffusion tensor magnetic resonance imaging (MRI).
Affective prosodic performance was assessed in 19 patients with schizophrenia and 19 comparison subjects with the Voice Emotion Identification Task (VOICEID), along with measures of basic pitch perception and executive processing (Wisconsin Card Sorting Test). Diffusion tensor MRI fractional anisotropy valves were used for voxelwise correlation analyses. In a follow-up experiment, performance on a nonaffective prosodic perception task was assessed in an additional cohort of 24 patients and 17 comparison subjects.
Patients showed significant deficits in VOICEID and Distorted Tunes Task performance. Impaired VOICEID performance correlated significantly with lower fractional anisotropy values within primary and secondary auditory pathways, orbitofrontal cortex, corpus callosum, and peri-amygdala white matter. Impaired Distorted Tunes Task performance also correlated with lower fractional anisotropy in auditory and amygdalar pathways but not prefrontal cortex. Wisconsin Card Sorting Test performance in schizophrenia correlated primarily with prefrontal fractional anisotropy. In the follow-up study, significant deficits were observed as well in nonaffective prosodic performance, along with significant intercorrelations among sensory, affective prosodic, and nonaffective measures.
Schizophrenia is associated with both structural and functional disturbances at the level of primary auditory cortex. Such deficits contribute significantly to patients' inability to decode both emotional and semantic aspects of speech, highlighting the importance of sensorial abnormalities in social communicatory dysfunction in schizophrenia.

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Available from: John J Foxe, Aug 27, 2015
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    • "Auditory cortex in the left hemisphere must integrate its sensory information with the homologous right hemisphere structures that process early prosodic cues, via the corpus callosum (Ross, 2010). The ability to perceive unimodal prosodic emotion cues alone has even been shown to relate to white matter integrity in the corpus callosum (Leitman et al., 2007). Although the potential for this left-right-hemisphere cooperation to go wrong is accepted at the theoretical level (Mitchell and Crow, 2005), there has so far only been one paper that has explicitly tested how neural processing of conflicting prosodic and semantic emotion cues is performed in schizophrenia. "
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    ABSTRACT: Our ability to make sense of emotional cues is of paramount importance for understanding state of mind and communicative intent. However, emotional cues often conflict with each other; this presents a significant challenge for people with schizophrenia. We conducted a theoretical review to determine the extent and types of impaired processing of emotion-related conflict in schizophrenia; we evaluated the relationship with medication and symptoms, and considered possible mediatory mechanisms. The literature established that people with schizophrenia demonstrated impaired function: (i) when passively exposed to emotion cues whilst performing an unrelated task, (ii) when selectively attending to one source of emotion cues whilst trying to ignore interference from another source, and (iii) when trying to resolve conflicting emotion cues and judge meta-communicative intent. These deficits showed associations with both negative and positive symptoms. There was limited evidence for antipsychotic medications attenuating impaired emotion perception when there are conflicting cues, with further direct research needed. Impaired attentional control and context processing may underlie some of the observed impairments. Neuroanatomical correlates are likely to involve interhemispheric transfer via the corpus callosum, limbic regions such as the amygdala, and possibly dorsolateral prefrontal and anterior cingulate cortex through their role in conflict processing.
    Psychiatry Research 08/2014; 220(1-2). DOI:10.1016/j.psychres.2014.07.077 · 2.68 Impact Factor
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    • "Negative symptoms have been shown to be associated with impaired social outcome (Leitman et al., 2005) and disorders of emotional prosody (Leitman et al., 2005, 2011). Emotional prosody deficits in schizophrenia involve reduced basic auditory sensory processing, as indicated by behavioral (Leitman et al., 2005, 2010) and electrophysiological (Jahshan et al., 2013) studies, and are associated with both structural and functional disturbances at the level of the primary auditory cortex (Leitman et al., 2007). Our findings are in accordance with these earlier results since they make the link between the efficacy of auditory processing in the temporal cortices (as indexed by P1 amplitude) and the severity of negative symptoms. "
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    ABSTRACT: Background Auditory verbal hallucinations (AVH) in schizophrenia may arise because of aberrant speech perception. We used an electroencephalography method to examine the neural processes underlying speech perception in schizophrenic patients with hallucinations. Methods Cortical event-related potentials (ERPs) were analyzed topographically (scalp potential and scalp current density (SCD) mapping) in response to the vowel /a/ using a passive paradigm in 26 patients with schizophrenia. Results From the SCD distribution of the P1 peak, we showed that, whereas the hallucination score (PSYRATS) was negatively correlated with the amplitude of the frontal currents, the PANSS negative symptom score was negatively correlated with the amplitude of the temporal currents in patients with schizophrenia. Conclusions These results provide evidence that AVH and negative symptoms are associated with abnormal early processing of speech. Whereas AVH are related to decreased early frontal activation, negative symptoms are associated with a reduced early temporal response.
    Schizophrenia Research 05/2014; 155(1-3). DOI:10.1016/j.schres.2014.03.007 · 4.43 Impact Factor
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    • "Further, pitch has been shown to be a key element that is manipulated to convey various emotions, along with amplitude and duration (Leitman et al., 2010b). A number of studies have demonstrated that schizophrenia patients have difficulty perceiving and discriminating emotions based on affective prosody (AP) cues, compared with controls (Murphy and Cutting, 1990; Kerr and Neale, 1993; Rabinowicz et al., 2000; Edwards et al., 2001; Rossell and Boundy, 2005; Bozikas et al., 2006; Leitman et al., 2007, 2010a; Shea et al., 2007; Kantrowitz et al., 2013). Further, there is increasing evidence to suggest that AVH status is associated with schizophrenia patients' performance in AP detection and discrimination: AVH patients have been found to perform worse on AP tasks than non-AVH schizophrenia patients (Rossell and Boundy, 2005; Shea et al., 2007; Rossell et al., in press). "
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    ABSTRACT: Research on auditory verbal hallucinations (AVHs) indicates that AVH schizophrenia patients show greater abnormalities on tasks requiring recognition of affective prosody (AP) than non-AVH patients. Detecting AP requires accurate perception of manipulations in pitch, amplitude and duration. Schizophrenia patients with AVHs also experience difficulty detecting these acoustic manipulations; with a number of theorists speculating that difficulties in pitch, amplitude and duration discrimination underlie AP abnormalities. This study examined whether both AP and these aspects of auditory processing are also impaired in first degree relatives of persons with AVHs. It also examined whether pitch, amplitude and duration discrimination were related to AP, and to hallucination proneness. Unaffected relatives of AVH schizophrenia patients (N=19) and matched healthy controls (N=33) were compared using tone discrimination tasks, an AP task, and clinical measures. Relatives were slower at identifying emotions on the AP task (p =.002), with secondary analysis showing this was especially so for happy (p = .014) and neutral (p =.001) sentences. There was a significant interaction effect for pitch between tone deviation level and group (p = .019), and relatives performed worse than controls on amplitude discrimination and duration discrimination. AP performance for happy and neutral sentences was significantly correlated with amplitude perception. Lastly, AVH proneness in the entire sample was significantly correlated with pitch discrimination (r = .44) and pitch perception was shown to predict AVH proneness in the sample (p = .005). These results suggest basic impairments in auditory processing are present in relatives of AVH patients; they potentially underlie processing speed in AP tasks, and predict AVH proneness. This indicates auditory processing deficits may be a core feature of AVHs in schizophrenia, and are worthy of further study as a potential endophenotype for AVHs.
    Frontiers in Human Neuroscience 09/2013; 7:531. DOI:10.3389/fnhum.2013.00531 · 2.90 Impact Factor
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