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Corollary Discharge Failure in an Oculomotor Task Is Related to Delusional Ideation in Healthy Individuals.

Malassis R, Del Cul A, Collins T - PLoS ONE (2015)

Bottom Line: Deficits in predictive activity, such as that afforded by a corollary discharge signal, have been reported in patients with schizophrenia, and may lead to the emergence of positive symptoms, in particular delusions of control and auditory hallucinations.Variation of the degree of self-generated movement knowledge as a function of the prevalence of delusional ideation in the normal population strongly supports the idea that corollary discharge deficits measured in schizophrenic patients in previous researches are not due to neuroleptic medication.We also propose that this difference in results between the perceptual and the motor tasks may point to a dissociation between corollary discharge for perception and corollary discharge for action.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire Psychologie de la Perception, Université Paris Descartes & CNRS, Paris, France.

ABSTRACT
Predicting the sensory consequences of saccadic eye movements likely plays a crucial role in planning sequences of saccades and in maintaining visual stability despite saccade-caused retinal displacements. Deficits in predictive activity, such as that afforded by a corollary discharge signal, have been reported in patients with schizophrenia, and may lead to the emergence of positive symptoms, in particular delusions of control and auditory hallucinations. We examined whether a measure of delusional thinking in the general, non-clinical population correlated with measures of predictive activity in two oculomotor tasks. The double-step task measured predictive activity in motor control, and the in-flight displacement task measured predictive activity in trans-saccadic visual perception. Forty-one healthy adults performed both tasks and completed a questionnaire to assess delusional thinking. The quantitative measure of predictive activity we obtained correlated with the tendency towards delusional ideation, but only for the motor task, and not the perceptual task: Individuals with higher levels of delusional thinking showed less self-movement information use in the motor task. Variation of the degree of self-generated movement knowledge as a function of the prevalence of delusional ideation in the normal population strongly supports the idea that corollary discharge deficits measured in schizophrenic patients in previous researches are not due to neuroleptic medication. We also propose that this difference in results between the perceptual and the motor tasks may point to a dissociation between corollary discharge for perception and corollary discharge for action.

No MeSH data available.


Related in: MedlinePlus

(A) Double-step task. After a 500–1000 ms fixation, the first target appeared for 250 ms, followed by a 250 ms blank (fixation target still on), the second target for 250 ms, another 250 ms blank. After an additional 200–400 ms, the fixation point turned off, indicating to the subjects that they were to perform their saccades. In the visually-guided version (not illustrated), the targets appeared successively and remained on until the end of the trial. (B) Possible target location combinations. First saccade targets appeared 10° to the left or right of the fixation point, second saccade targets above or below the first target. There were thus four patterns: left-up, left-down, right-up, right-down. The example illustrated the right-up pattern. (C) Sample traces from 2 subjects. Each line represents a single second saccade. For each subject, PDI score and the slope from regression between the first saccade error and second saccade horizontal component (see Results section).
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pone.0134483.g001: (A) Double-step task. After a 500–1000 ms fixation, the first target appeared for 250 ms, followed by a 250 ms blank (fixation target still on), the second target for 250 ms, another 250 ms blank. After an additional 200–400 ms, the fixation point turned off, indicating to the subjects that they were to perform their saccades. In the visually-guided version (not illustrated), the targets appeared successively and remained on until the end of the trial. (B) Possible target location combinations. First saccade targets appeared 10° to the left or right of the fixation point, second saccade targets above or below the first target. There were thus four patterns: left-up, left-down, right-up, right-down. The example illustrated the right-up pattern. (C) Sample traces from 2 subjects. Each line represents a single second saccade. For each subject, PDI score and the slope from regression between the first saccade error and second saccade horizontal component (see Results section).

Mentions: The first visuo-motor task was the double-step task [19], in which two visual targets are flashed successively on a screen (Fig 1A and 1B). Subjects are asked to perform memory-guided saccades to the remembered locations of the targets. Performing the first saccade is relatively easy, and requires only transforming the visual information about target location into a motor vector appropriate for guiding a saccade. If the second saccade applied the same sensory-motor transformation, however, the second saccade would grossly miss the (remembered) target location because the eyes have moved since the visual information was encoded. Correct second saccades therefore require information about the first saccade to be combined with the remembered second target location. The fact that humans and macaque monkeys perform the double-step task with ease is evidence in favor of a self-movement, or corollary discharge-like signal (CD) being used in this task. It is also possible to obtain a quantitative measure of CD information use in this task, by examining the relationship between first and second saccade errors [20–22]. Indeed, if the saccadic system possesses specific metric information about the first saccade, then the size of the second saccade should correlate with the first saccade because it would correct for targeting errors occurring on the first saccade. If no CD information contributes to the second saccade, then first and second saccade amplitudes will be independent. The correlation coefficient is therefore an index of CD information use in the double-step task.


Corollary Discharge Failure in an Oculomotor Task Is Related to Delusional Ideation in Healthy Individuals.

Malassis R, Del Cul A, Collins T - PLoS ONE (2015)

(A) Double-step task. After a 500–1000 ms fixation, the first target appeared for 250 ms, followed by a 250 ms blank (fixation target still on), the second target for 250 ms, another 250 ms blank. After an additional 200–400 ms, the fixation point turned off, indicating to the subjects that they were to perform their saccades. In the visually-guided version (not illustrated), the targets appeared successively and remained on until the end of the trial. (B) Possible target location combinations. First saccade targets appeared 10° to the left or right of the fixation point, second saccade targets above or below the first target. There were thus four patterns: left-up, left-down, right-up, right-down. The example illustrated the right-up pattern. (C) Sample traces from 2 subjects. Each line represents a single second saccade. For each subject, PDI score and the slope from regression between the first saccade error and second saccade horizontal component (see Results section).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4549245&req=5

pone.0134483.g001: (A) Double-step task. After a 500–1000 ms fixation, the first target appeared for 250 ms, followed by a 250 ms blank (fixation target still on), the second target for 250 ms, another 250 ms blank. After an additional 200–400 ms, the fixation point turned off, indicating to the subjects that they were to perform their saccades. In the visually-guided version (not illustrated), the targets appeared successively and remained on until the end of the trial. (B) Possible target location combinations. First saccade targets appeared 10° to the left or right of the fixation point, second saccade targets above or below the first target. There were thus four patterns: left-up, left-down, right-up, right-down. The example illustrated the right-up pattern. (C) Sample traces from 2 subjects. Each line represents a single second saccade. For each subject, PDI score and the slope from regression between the first saccade error and second saccade horizontal component (see Results section).
Mentions: The first visuo-motor task was the double-step task [19], in which two visual targets are flashed successively on a screen (Fig 1A and 1B). Subjects are asked to perform memory-guided saccades to the remembered locations of the targets. Performing the first saccade is relatively easy, and requires only transforming the visual information about target location into a motor vector appropriate for guiding a saccade. If the second saccade applied the same sensory-motor transformation, however, the second saccade would grossly miss the (remembered) target location because the eyes have moved since the visual information was encoded. Correct second saccades therefore require information about the first saccade to be combined with the remembered second target location. The fact that humans and macaque monkeys perform the double-step task with ease is evidence in favor of a self-movement, or corollary discharge-like signal (CD) being used in this task. It is also possible to obtain a quantitative measure of CD information use in this task, by examining the relationship between first and second saccade errors [20–22]. Indeed, if the saccadic system possesses specific metric information about the first saccade, then the size of the second saccade should correlate with the first saccade because it would correct for targeting errors occurring on the first saccade. If no CD information contributes to the second saccade, then first and second saccade amplitudes will be independent. The correlation coefficient is therefore an index of CD information use in the double-step task.

Bottom Line: Deficits in predictive activity, such as that afforded by a corollary discharge signal, have been reported in patients with schizophrenia, and may lead to the emergence of positive symptoms, in particular delusions of control and auditory hallucinations.Variation of the degree of self-generated movement knowledge as a function of the prevalence of delusional ideation in the normal population strongly supports the idea that corollary discharge deficits measured in schizophrenic patients in previous researches are not due to neuroleptic medication.We also propose that this difference in results between the perceptual and the motor tasks may point to a dissociation between corollary discharge for perception and corollary discharge for action.

View Article: PubMed Central - PubMed

Affiliation: Laboratoire Psychologie de la Perception, Université Paris Descartes & CNRS, Paris, France.

ABSTRACT
Predicting the sensory consequences of saccadic eye movements likely plays a crucial role in planning sequences of saccades and in maintaining visual stability despite saccade-caused retinal displacements. Deficits in predictive activity, such as that afforded by a corollary discharge signal, have been reported in patients with schizophrenia, and may lead to the emergence of positive symptoms, in particular delusions of control and auditory hallucinations. We examined whether a measure of delusional thinking in the general, non-clinical population correlated with measures of predictive activity in two oculomotor tasks. The double-step task measured predictive activity in motor control, and the in-flight displacement task measured predictive activity in trans-saccadic visual perception. Forty-one healthy adults performed both tasks and completed a questionnaire to assess delusional thinking. The quantitative measure of predictive activity we obtained correlated with the tendency towards delusional ideation, but only for the motor task, and not the perceptual task: Individuals with higher levels of delusional thinking showed less self-movement information use in the motor task. Variation of the degree of self-generated movement knowledge as a function of the prevalence of delusional ideation in the normal population strongly supports the idea that corollary discharge deficits measured in schizophrenic patients in previous researches are not due to neuroleptic medication. We also propose that this difference in results between the perceptual and the motor tasks may point to a dissociation between corollary discharge for perception and corollary discharge for action.

No MeSH data available.


Related in: MedlinePlus