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: 12.3). 04/2007; 164(3):474-82. DOI: 10.1176/appi.ajp.164.3.474
Source: PubMed


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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    • "In Table I language deficits in schizophrenia are tentatively summarized along with the description of the potential neural networks involved, as detected by functional and diffusion imaging studies (Kircher et al., 2005; 2007; Leitman et al., 2007; Park et al., 2008; Andreasen et al., 2008). "

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    • "The first explanation refers to the sensory deficit in schizophrenia. Several studies have reported a basic sensory disturbance in the processing of emotion in the facial (Turetsky et al., 2007; Wynn et al., 2008; Norton et al., 2009; Laprevote et al., 2010; McBain et al., 2010; Bedwell et al., 2013; Jahshan et al., 2013) and vocal (Leitman et al., 2005, 2007, 2010, 2011a; Gold et al., 2012; Kantrowitz et al., 2013) modalities. This is unlikely to be the case in our study since patients with basic sensory disturbances, as assessed with the Benton test and the PEGA, were excluded from our sample. "
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    ABSTRACT: There has been extensive research on impaired emotion recognition in schizophrenia in the facial and vocal modalities. The literature points to biases toward non-relevant emotions for emotional faces but few studies have examined biases in emotional recognition across different modalities (facial and vocal). In order to test emotion recognition biases, we exposed 23 patients with stabilized chronic schizophrenia and 23 healthy controls (HCs) to emotional facial and vocal tasks asking them to rate emotional intensity on visual analog scales. We showed that patients with schizophrenia provided higher intensity ratings on the non-target scales (e.g., surprise scale for fear stimuli) than HCs for the both tasks. Furthermore, with the exception of neutral vocal stimuli, they provided the same intensity ratings on the target scales as the HCs. These findings suggest that patients with chronic schizophrenia have emotional biases when judging emotional stimuli in the visual and vocal modalities. These biases may stem from a basic sensorial deficit, a high-order cognitive dysfunction, or both. The respective roles of prefrontal-subcortical circuitry and the basal ganglia are discussed.
    Full-text · Article · Aug 2014 · Frontiers in Psychology
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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.
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