Anatomical and physiological evidence for a relationship between the ‘cingular’ vocalization area and the auditory cortex in the squirrel monkey

doi:10.1016/0006-8993(80)90143-2

Brain Research

Volume 202, Issue 2, 8 December 1980, Pages 307-315

https://doi.org/10.1016/0006-8993(80)90143-2 Get rights and content

Abstract

With the aid of the autoradiographic tracing technique the projections from cortical limbic vocalization areas to the auditory cortex in the superior temporal gyrus were studied in the squirrel monkey. The vocalization areas were identified by exploring the anterior limbic cortex with moving electrodes until a site was found where electrical stimulation yielded vocalization. Projections from the region around the cingulate sulcus and supracallosal anterior cingulate gyrus have their terminal fields in the lower part of the superior temporal gyrus (STG) and upper bank of the superior temporal sulcus. Injections just in front of the genu of the corpus callosum and in the subcallosal gyrus and gyrus rectus lead to terminal fields in the middle part of STG. No projections were found in the upper part of STG, i.e. the primary auditory cortex.

To test the functional properties of this pathway, action potentials of single neurons in the auditory cortex were recorded during electrical stimulation of the cingular vocalization area. From a total of 135 STG neurons, an effect on spontaneous activity was seen in 27 cells. All except one of these neurons also reacted to acoustic stimuli. In most cases, stimulation of the cingular area caused a decrease in the discharge rate of the STG neurons. In 4 neurons, stimulation of the vocalization area had an influence on the acoustic reactivity of the STG neurons. The results provide evidence that during phonation the ‘cingular’ vocalization area exerts a predominantly inhibitory influence on auditory cortex neurons. This effect probably is mediated via the extreme capsule. Its possible function is discussed.

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Citation Excerpt :
There is also evidence that bidirectional anatomic connections exist between the frontal lobe and auditory cortex in both marmosets (60,67) and macaques (68,69). Stimulation of frontal cortex in primates can evoke inhibition in auditory cortex (70,71), but whether such connections are active during vocalization is unknown. Additionally, many of these frontal cortex regions, particularly the premotor cortex, exhibit both vocal premotor activity and auditory responses (30,62,66,72,73), making the frontal cortex a region of interest as a possible source for corollary discharge signals as well as a possible recipient area of auditory cortex vocal outputs.
Interactions between motor systems and sensory processing are ubiquitous throughout the animal kingdom and play an important role in many sensorimotor behaviors, including both human speech and animal vocalization. During vocal production, the auditory system plays important roles in both encoding feedback of produced sounds, allowing one to self-monitor for vocal errors, and simultaneously maintaining sensitivity to the outside acoustic environment. Supporting these roles is an efferent motor-to-sensory signal known as a corollary discharge. This review summarizes recent work on the role of such signaling during vocalization in the marmoset monkey, a nonhuman primate model of social vocal communication.
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Mouse vocal communication system: Are ultrasounds learned or innate?
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Mouse ultrasonic vocalizations (USVs) are often used as behavioral readouts of internal states, to measure effects of social and pharmacological manipulations, and for behavioral phenotyping of mouse models for neuropsychiatric and neurodegenerative disorders. However, little is known about the neurobiological mechanisms of rodent USV production. Here we discuss the available data to assess whether male mouse song behavior and the supporting brain circuits resemble those of known vocal non-learning or vocal learning species. Recent neurobiology studies have demonstrated that the mouse USV brain system includes motor cortex and striatal regions, and that the vocal motor cortex sends a direct sparse projection to the brainstem vocal motor nucleus ambiguous, a projection previously thought be unique to humans among mammals. Recent behavioral studies have reported opposing conclusions on mouse vocal plasticity, including vocal ontogeny changes in USVs over early development that might not be explained by innate maturation processes, evidence for and against a role for auditory feedback in developing and maintaining normal mouse USVs, and evidence for and against limited vocal imitation of song pitch. To reconcile these findings, we suggest that the trait of vocal learning may not be dichotomous but encompass a broad spectrum of behavioral and neural traits we call the continuum hypothesis, and that mice possess some of the traits associated with a capacity for limited vocal learning.
The effect of gender on the N1-P2 auditory complex while listening and speaking with altered auditory feedback
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The effect of gender on the N1–P2 auditory complex was examined while listening and speaking with altered auditory feedback. Fifteen normal hearing adult males and 15 females participated. N1–P2 components were evoked while listening to self-produced nonaltered and frequency shifted /a/ tokens and during production of /a/ tokens during nonaltered auditory feedback (NAF), frequency altered feedback (FAF), and delayed auditory feedback (DAF; 50 and 200 ms). During speech production, females exhibited earlier N1 latencies during 50 ms DAF and earlier P2 latencies during 50 ms DAF and FAF. There were no significant differences in N1–P2 amplitudes across all conditions. Comparing listening to active speaking, N1 and P2 latencies were earlier among females, with speaking, and under NAF. N1–P2 amplitudes were significantly reduced during speech production. These findings are consistent with the notions that speech production suppresses auditory cortex responsiveness and males and females process altered auditory feedback differently while speaking.
One year longitudinal study of the straight gyrus morphometry in first-episode schizophrenia-spectrum patients
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The SG is situated medially to the olfactory groove (olfactory sulcus) at the ventromedial edge of the frontal lobe, and is considered to be the frontal extension of the anterior cingulate gyrus. Animal studies have reported that the SG is a part of the anterior limbic system and is specifically connected to auditory cortex neurons in the convexity of the superior temporal gyrus (Müeller-Preuss et al., 1980). In line with other studies (Szendi et al., 2006; Takayanagi et al., 2010), we have reported that SG morphometry did not significantly differ between healthy subjects and schizophrenia spectrum patients at the onset of psychosis (Roiz-Santiañez et al., 2011).
Effects of voice harmonic complexity on ERP responses to pitch-shifted auditory feedback
2011, Clinical Neurophysiology
Citation Excerpt :
In addition to the arguments presented above, and despite the possibility of complex interactions between bone-conducted and auditory feedback, results of the present study are in agreement with several other studies that have shown that the activity of the vocal motor system modulates (either enhances or suppresses) the sensory neural processing of auditory feedback. Early studies in primates have shown that electrically-induced activation of the vocal motor system modulates (suppresses) the activity of cortical auditory neurons (Müller-Preuss et al., 1980; Muller-Preuss and Ploog, 1981). The motor-induced suppression effect was also reported in the auditory system during voluntary vocalizations in humans and primates (Eliades and Wang, 2003; Heinks-Maldonado et al., 2005; Houde et al., 2002).
The present study investigated the neural mechanisms of voice pitch control for different levels of harmonic complexity in the auditory feedback.
Event-related potentials (ERPs) were recorded in response to +200 cents pitch perturbations in the auditory feedback of self-produced natural human vocalizations, complex and pure tone stimuli during active vocalization and passive listening conditions.
During active vocal production, ERP amplitudes were largest in response to pitch shifts in the natural voice, moderately large for non-voice complex stimuli and smallest for the pure tones. However, during passive listening, neural responses were equally large for pitch shifts in voice and non-voice complex stimuli but still larger than that for pure tones.
These findings suggest that pitch change detection is facilitated for spectrally rich sounds such as natural human voice and non-voice complex stimuli compared with pure tones. Vocalization-induced increase in neural responses for voice feedback suggests that sensory processing of naturally-produced complex sounds such as human voice is enhanced by means of motor-driven mechanisms (e.g. efference copies) during vocal production.
This enhancement may enable the audio-vocal system to more effectively detect and correct for vocal errors in the feedback of natural human vocalizations to maintain an intended vocal output for speaking.

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Brain Research

Abstract

References (23)

Convergence of prefrontal and acoustic inputs upon neurons in the superior temporal gyrus of the awake squirrel monkey

Brain Research

Bilateral temporofrontal projections in the squirrel monkey: origin, distribution and pathways

Brain Research

The autoradiographic demonstration of axonal connections in the central nervous system

Brain Research

Projections from the cingular vocalization area in the squirrel monkey

Brain Research

Multiple coding of species-specific vocalizations in the auditory cortex of squirrel monkeys

Brain Research

Intra- and interhemispheric connections of the neocortical auditory system in the rhesus monkey

Brain Research

Efferent cortico-cortical projections of the prefrontal cortex in the rhesus monkey

Brain Research

Vocalization evoked from forebrain in Macaca mulatta

Physiol. Behav.

Neocortical and limbic lesion effects on primate phonation

Brain Research

The effect of superior temporal lesions on the recognition of species-specific calls in the squirrel monkey

Exp. Brain Res.

Some cortical association systems related to auditory functions

J. comp. Neurol.

Cited by (82)

Corollary Discharge Mechanisms During Vocal Production in Marmoset Monkeys

Cingulate Cortex and Pain Architecture

Mouse vocal communication system: Are ultrasounds learned or innate?

The effect of gender on the N1-P2 auditory complex while listening and speaking with altered auditory feedback

One year longitudinal study of the straight gyrus morphometry in first-episode schizophrenia-spectrum patients

Effects of voice harmonic complexity on ERP responses to pitch-shifted auditory feedback