Not pitch perfect: Sensory contributions to affective communication impairment in schizophrenia

David I. Leitman, Daniel H. Wolf, Petri Laukka, John D Ragland, Jeffrey N. Valdez, Bruce I. Turetsky, Raquel E. Gur, Ruben C. Gur

Research output: Contribution to journalArticle

37 Citations (Scopus)

Abstract

Background: Schizophrenia patients have vocal affect (prosody) deficits that are treatment resistant and associated with negative symptoms and poor outcome. The neural correlates of this dysfunction are unclear. Prior study has suggested that schizophrenia vocal affect perception deficits stem from an inability to use acoustic cues, notably pitch, in decoding emotion. Methods: Functional magnetic resonance imaging was performed in 24 schizophrenia patients and 28 healthy control subjects, during the performance of a four-choice (happiness, fear, anger, neutral) vocal affect identification task in which items for each emotion varied parametrically in affective salient acoustic cue levels. Results: We observed that parametric increases in cue levels in schizophrenia failed to produce the same identification rate increases as in control subjects. These deficits correlated with diminished reciprocal activation changes in superior temporal and inferior frontal gyri and reduced temporo-frontal connectivity. Task activation also correlated with independent measures of pitch perception and negative symptom severity. Conclusions: These findings illustrate the interplay between sensory and higher-order cognitive dysfunction in schizophrenia. Sensory contributions to vocal affect deficits also suggest that this neurobehavioral marker could be targeted by pharmacological or behavioral remediation of acoustic feature discrimination.

Original languageEnglish (US)
Pages (from-to)611-618
Number of pages8
JournalBiological Psychiatry
Volume70
Issue number7
DOIs
StatePublished - Oct 1 2011

Fingerprint

Schizophrenia
Communication
Acoustics
Cues
Prefrontal Cortex
Emotions
Pitch Perception
Happiness
Anger
Fear
Healthy Volunteers
Magnetic Resonance Imaging
Pharmacology
Therapeutics

Keywords

  • Emotion
  • fMRI
  • inferior frontal gyrus
  • schizophrenia
  • speech
  • temporal cortex

ASJC Scopus subject areas

  • Biological Psychiatry

Cite this

Not pitch perfect : Sensory contributions to affective communication impairment in schizophrenia. / Leitman, David I.; Wolf, Daniel H.; Laukka, Petri; Ragland, John D; Valdez, Jeffrey N.; Turetsky, Bruce I.; Gur, Raquel E.; Gur, Ruben C.

In: Biological Psychiatry, Vol. 70, No. 7, 01.10.2011, p. 611-618.

Research output: Contribution to journalArticle

Leitman, DI, Wolf, DH, Laukka, P, Ragland, JD, Valdez, JN, Turetsky, BI, Gur, RE & Gur, RC 2011, 'Not pitch perfect: Sensory contributions to affective communication impairment in schizophrenia', Biological Psychiatry, vol. 70, no. 7, pp. 611-618. https://doi.org/10.1016/j.biopsych.2011.05.032
Leitman, David I. ; Wolf, Daniel H. ; Laukka, Petri ; Ragland, John D ; Valdez, Jeffrey N. ; Turetsky, Bruce I. ; Gur, Raquel E. ; Gur, Ruben C. / Not pitch perfect : Sensory contributions to affective communication impairment in schizophrenia. In: Biological Psychiatry. 2011 ; Vol. 70, No. 7. pp. 611-618.
@article{406a016a68c0428f92f26904cfa8cb42,
title = "Not pitch perfect: Sensory contributions to affective communication impairment in schizophrenia",
abstract = "Background: Schizophrenia patients have vocal affect (prosody) deficits that are treatment resistant and associated with negative symptoms and poor outcome. The neural correlates of this dysfunction are unclear. Prior study has suggested that schizophrenia vocal affect perception deficits stem from an inability to use acoustic cues, notably pitch, in decoding emotion. Methods: Functional magnetic resonance imaging was performed in 24 schizophrenia patients and 28 healthy control subjects, during the performance of a four-choice (happiness, fear, anger, neutral) vocal affect identification task in which items for each emotion varied parametrically in affective salient acoustic cue levels. Results: We observed that parametric increases in cue levels in schizophrenia failed to produce the same identification rate increases as in control subjects. These deficits correlated with diminished reciprocal activation changes in superior temporal and inferior frontal gyri and reduced temporo-frontal connectivity. Task activation also correlated with independent measures of pitch perception and negative symptom severity. Conclusions: These findings illustrate the interplay between sensory and higher-order cognitive dysfunction in schizophrenia. Sensory contributions to vocal affect deficits also suggest that this neurobehavioral marker could be targeted by pharmacological or behavioral remediation of acoustic feature discrimination.",
keywords = "Emotion, fMRI, inferior frontal gyrus, schizophrenia, speech, temporal cortex",
author = "Leitman, {David I.} and Wolf, {Daniel H.} and Petri Laukka and Ragland, {John D} and Valdez, {Jeffrey N.} and Turetsky, {Bruce I.} and Gur, {Raquel E.} and Gur, {Ruben C.}",
year = "2011",
month = "10",
day = "1",
doi = "10.1016/j.biopsych.2011.05.032",
language = "English (US)",
volume = "70",
pages = "611--618",
journal = "Biological Psychiatry",
issn = "0006-3223",
publisher = "Elsevier USA",
number = "7",

}

TY - JOUR

T1 - Not pitch perfect

T2 - Sensory contributions to affective communication impairment in schizophrenia

AU - Leitman, David I.

AU - Wolf, Daniel H.

AU - Laukka, Petri

AU - Ragland, John D

AU - Valdez, Jeffrey N.

AU - Turetsky, Bruce I.

AU - Gur, Raquel E.

AU - Gur, Ruben C.

PY - 2011/10/1

Y1 - 2011/10/1

N2 - Background: Schizophrenia patients have vocal affect (prosody) deficits that are treatment resistant and associated with negative symptoms and poor outcome. The neural correlates of this dysfunction are unclear. Prior study has suggested that schizophrenia vocal affect perception deficits stem from an inability to use acoustic cues, notably pitch, in decoding emotion. Methods: Functional magnetic resonance imaging was performed in 24 schizophrenia patients and 28 healthy control subjects, during the performance of a four-choice (happiness, fear, anger, neutral) vocal affect identification task in which items for each emotion varied parametrically in affective salient acoustic cue levels. Results: We observed that parametric increases in cue levels in schizophrenia failed to produce the same identification rate increases as in control subjects. These deficits correlated with diminished reciprocal activation changes in superior temporal and inferior frontal gyri and reduced temporo-frontal connectivity. Task activation also correlated with independent measures of pitch perception and negative symptom severity. Conclusions: These findings illustrate the interplay between sensory and higher-order cognitive dysfunction in schizophrenia. Sensory contributions to vocal affect deficits also suggest that this neurobehavioral marker could be targeted by pharmacological or behavioral remediation of acoustic feature discrimination.

AB - Background: Schizophrenia patients have vocal affect (prosody) deficits that are treatment resistant and associated with negative symptoms and poor outcome. The neural correlates of this dysfunction are unclear. Prior study has suggested that schizophrenia vocal affect perception deficits stem from an inability to use acoustic cues, notably pitch, in decoding emotion. Methods: Functional magnetic resonance imaging was performed in 24 schizophrenia patients and 28 healthy control subjects, during the performance of a four-choice (happiness, fear, anger, neutral) vocal affect identification task in which items for each emotion varied parametrically in affective salient acoustic cue levels. Results: We observed that parametric increases in cue levels in schizophrenia failed to produce the same identification rate increases as in control subjects. These deficits correlated with diminished reciprocal activation changes in superior temporal and inferior frontal gyri and reduced temporo-frontal connectivity. Task activation also correlated with independent measures of pitch perception and negative symptom severity. Conclusions: These findings illustrate the interplay between sensory and higher-order cognitive dysfunction in schizophrenia. Sensory contributions to vocal affect deficits also suggest that this neurobehavioral marker could be targeted by pharmacological or behavioral remediation of acoustic feature discrimination.

KW - Emotion

KW - fMRI

KW - inferior frontal gyrus

KW - schizophrenia

KW - speech

KW - temporal cortex

UR - http://www.scopus.com/inward/record.url?scp=80052839240&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80052839240&partnerID=8YFLogxK

U2 - 10.1016/j.biopsych.2011.05.032

DO - 10.1016/j.biopsych.2011.05.032

M3 - Article

C2 - 21762876

AN - SCOPUS:80052839240

VL - 70

SP - 611

EP - 618

JO - Biological Psychiatry

JF - Biological Psychiatry

SN - 0006-3223

IS - 7

ER -