Neocortical and limbic lesion effects on primate phonation

doi:10.1016/0006-8993(74)90191-7

Brain Research

Volume 71, Issue 1, 10 May 1974, Pages 61-75

https://doi.org/10.1016/0006-8993(74)90191-7 Get rights and content

Abstract

Five monkeys were individually trained to emit a relatively prolonged call of specified loudness in order to obtain a preferred food. At the completion of training each animal gave the required call in response to a signal cue light and withheld calls during periods in which no cue light was present.

Sequential bilateral removal of the homolog of Broca's area, transitional parieto-occipital cortex, and temporal association cortex in 3 monkeys had no influence on performance of the discriminative call. There was no change in sound spectral properties of the call as a result of surgery.

Bilateral removal of anterior cingulate/subcallosal gyrus in the remaining two monkeys was accompanied by loss of phonatory performance. Postoperative calls given by each of these animals in the test situation were weak and infrequent.

The data indicate that control over learned, discriminative phonation in monkeys is not mediated by neorcortical regions homologous to human ‘speech’ areas.

Reference (31)

FranzenE.A. et al.
Neural control of social behavior: prefrontal and anterior temporal cortex
Neuropsychologia
(1973)
HughesJ.R. et al.
Studies on the supracallosal mesial cortex of unanesthetized, conscious mammals. II. Monkey. A. Movements elicited by electrical stimulation
Electroenceph. clin. Neurophysiol.
(1962)
O'BrienJ.H. et al.
Evoked cortical responses to vagal, laryngeal and facial afferents in monkeys under chloralose anesthesia
Electroenceph. clin. Neurophysiol.
(1971)
RobinsonB.W.
Localization evoked from forebrain inMacaca mulatta
Physiol. Behav.
(1967)
SuttonD. et al.
Vocalization in rhesus monkeys: conditionability
Brain Research
(1973)
TalairachJ. et al.
The cingulate gyrus and human behavior
Electroenceph. clin. Neurophysiol.
(1973)
AndrewR.J.
The situations that evoke vocalization in primates
Ann. N.Y. Acad. Sci.
(1962)
ApfelbachR.
Electrically elicited vocalizations in the gibbonHylobates lar (Hylobatidae), and their behavioral significance
Z. Tierpsychol.
(1972)
BarrisR.W. et al.
Bilateral anterior cingulate gyrus lesions
Neurology (Minneap.)
(1953)
BotezM.I. et al.
Role of subcortical structures and particularly of the thalamus in mechanisms of speech and language
Int. J. Neurol.
(1971)

Dusser de BarenneJ.G. et al.

The ‘motor’ cortex of the chimpanzee

J. Neurophysiol.

(1941)

GleesP. et al.

The effects of lesions in the cingular gyrus and adjacent areas in monkeys

J. Neurol. Neurosurg. Psychiat.

(1950)

GreenH.D. et al.

The effects of ablation of the cortical motor face area in monkeys

J. Neurophysiol.

(1938)

HastM.H. et al.

The response of the vocal folds to electrical stimulation of inferior frontal cortex

Acta oto-laryng. (Stockh.)

(1966)

JurgensU. et al.

Vocalization in the squirrel monkey (Saimiri sciureus) elicited by brain stimulation

Exp. Brain Res.

(1967)

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Neocortical and limbic lesion effects on primate phonation

Abstract

Neuropsychologia

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Physiol. Behav.

Brain Research

Electroenceph. clin. Neurophysiol.

The situations that evoke vocalization in primates

Ann. N.Y. Acad. Sci.

Electrically elicited vocalizations in the gibbonHylobates lar (Hylobatidae), and their behavioral significance

Z. Tierpsychol.

Bilateral anterior cingulate gyrus lesions

Neurology (Minneap.)

Role of subcortical structures and particularly of the thalamus in mechanisms of speech and language

Int. J. Neurol.

The ‘motor’ cortex of the chimpanzee

J. Neurophysiol.

The effects of lesions in the cingular gyrus and adjacent areas in monkeys

J. Neurol. Neurosurg. Psychiat.

The effects of ablation of the cortical motor face area in monkeys

J. Neurophysiol.

The response of the vocal folds to electrical stimulation of inferior frontal cortex

Acta oto-laryng. (Stockh.)

Vocalization in the squirrel monkey (Saimiri sciureus) elicited by brain stimulation

Exp. Brain Res.