It has been well documented that neurons in the auditory cortex of anaesthetized animals generally display transient responses to acoustic stimulation, and typically respond to a brief stimulus with one or fewer action potentials. The number of action potentials evoked by each stimulus usually does not increase with increasing stimulus duration. Such observations have long puzzled researchers across disciplines and raised serious questions regarding the role of the auditory cortex in encoding ongoing acoustic signals. Contrary to these long-held views, here we show that single neurons in both primary (area A1) and lateral belt areas of the auditory cortex of awake marmoset monkeys (Callithrix jacchus) are capable of firing in a sustained manner over a prolonged period of time, especially when they are driven by their preferred stimuli. In contrast, responses become more transient or phasic when auditory cortex neurons respond to non-preferred stimuli. These findings suggest that when the auditory cortex is stimulated by a sound, a particular population of neurons fire maximally throughout the duration of the sound. Responses of other, less optimally driven neurons fade away quickly after stimulus onset. This results in a selective representation of the sound across both neuronal population and time.

We investigated neural coding of sinusoidally modulated tones (sAM and sFM) in the primary auditory cortex (A1) of awake marmoset monkeys, demonstrating that there are systematic cortical representations of embedded temporal features that are based on both average discharge rate and stimulus-synchronized discharge patterns. The rate-representation appears to be coded alongside the stimulus-synchronized discharges, such that the auditory cortex has access to both rate and temporal representations of the stimulus at high and low frequencies, respectively. Furthermore, we showed that individual auditory cortical neurons, as well as populations of neurons, have common features in their responses to both sAM and sFM stimuli. These results may explain the similarities in the perception of sAM and sFM stimuli as well as the different perceptual qualities effected by different modulation frequencies. The main findings include the following. 1) Responses of cortical neurons to sAM and sFM stimuli in awake marmosets were generally much stronger than responses to unmodulated tones. Some neurons responded to sAM or sFM stimuli but not to pure tones. 2) The discharge rate-based modulation transfer function typically had a band-pass shape and was centered at a preferred modulation frequency (rBMF). Population-averaged mean firing rate peaked at 16- to 32-Hz modulation frequency, indicating that the A1 was maximally excited by this frequency range of temporal modulations. 3) Only approximately 60% of recorded units showed statistically significant discharge synchrony to the modulation waveform of sAM or sFM stimuli. The discharge synchrony-based best modulation frequency (tBMF) was typically lower than the rBMF measured from the same neuron. The distribution of rBMF over the population of neurons was approximately one octave higher than the distribution of tBMF. 4) There was a high degree of similarity between cortical responses to sAM and sFM stimuli that was reflected in both discharge rate- or synchrony-based response measures. 5) Inhibition appeared to be a contributing factor in limiting responses at modulation frequencies above the rBMF of a neuron. And 6) neurons with shorter response latencies tended to have higher tBMF and maximum discharge synchrony frequency than those with longer response latencies. rBMF was not significantly correlated with the minimum response latency.

The representation of rapid acoustic transients by the auditory cortex is a fundamental issue that is still unresolved. Auditory cortical neurons have been shown to be limited in their stimulus-synchronized responses, yet the perceptual performances of humans and animals in discriminating temporal variations in complex sounds are better than what existing neurophysiological data would predict. This study investigated the neural representation of temporally asymmetric stimuli in the primary auditory cortex of awake marmoset monkeys. The stimuli, ramped and damped sinusoids, were systematically manipulated (by means of half-life of the exponential envelope) within a cortical neuron's presumed temporal integration window. The main findings of this study are as follows: 1) temporal asymmetry in ramped and damped sinusoids with a short period (25 ms) was clearly reflected by average discharge rate but not necessarily by temporal discharge patterns of auditory cortical neurons. There was considerable response specificity to these stimuli such that some neurons were strongly responsive to a ramped sinusoid but almost completely unresponsive to its damped counterpart or vice versa. Of 181 neurons studied, 140 (77%) showed significant response asymmetry in at least one of the tested half-life values of the exponential envelope. Forty-six neurons showed significant response asymmetry over all half-lives tested. Sustained firing, commonly observed under awake conditions, contributed to greater response asymmetry than that of onset responses in many neurons. 2) A greater proportion of the neurons (32/46) that exhibited significant overall response asymmetry showed stronger responses to the ramped sinusoids than to the damped sinusoids, possibly contributing to the difference in the perceived loudness between these two classes of sounds. 3) The asymmetry preference of a neuron to ramped or damped sinusoids did not appear to be correlated with its characteristic frequency or minimum response latency, suggesting that this is a general phenomenon that exists across populations of cortical neurons. Moreover, the intensity of the stimuli did not have significant effects on the measure of the asymmetry preference based on discharge rate. 4) A population measure of response preference, based on discharge rate, of cortical neurons to the temporally asymmetric stimuli was qualitatively similar to the performance of human listeners in discriminating ramped versus damped sinusoids at different half-life values. These findings suggest that rapid acoustic transients embedded in complex sounds can be represented by discharge rates of cortical neurons instead of or in the absence of stimulus-synchronized discharges.

A number of studies in various species have demonstrated that natural vocalizations generally produce stronger neural responses than do their time-reversed versions. The majority of neurons in the primary auditory cortex (A1) of marmoset monkeys responds more strongly to natural marmoset vocalizations than to the time-reversed vocalizations. However, it was unclear whether such differences in neural responses were simply due to the difference between the acoustic structures of natural and time-reversed vocalizations or whether they also resulted from the difference in behavioral relevance of both types of the stimuli. To address this issue, we have compared neural responses to natural and time-reversed marmoset twitter calls in A1 of cats with those obtained from A1 of marmosets using identical stimuli. It was found that the preference for natural marmoset twitter calls demonstrated in marmoset A1 was absent in cat A1. While both cortices responded approximately equally to time-reversed twitter calls, marmoset A1 responded much more strongly to natural twitter calls than did cat A1. This differential representation of marmoset vocalizations in two cortices suggests that experience-dependent and possibly species-specific mechanisms are involved in cortical processing of communication sounds.

Single neurons in the primate auditory cortex exhibit vocalization-related modulations (excitatory or inhibitory) during self-initiated vocal production. Previous studies have shown that these modulations of cortical activity are variable in individual neurons' responses to multiple instances of vocalization and diverse between different cortical neurons. The present study investigated dynamic patterns of vocalization-related modulations and demonstrated that much of the variability in cortical modulations was related to the acoustic structures of self-produced vocalization. We found that suppression of single unit activity during multi-phrased vocalizations was temporally specific in that it was maintained during each phrase, but was released between phrases. Furthermore, the degree of suppression or excitation was correlated to the mean energy and frequency of the produced vocalizations, accounting for much of the response variability between multiple instances of vocalization. Simultaneous recordings of pairs of neurons from a single electrode revealed that the modulations by self-produced vocalizations in nearby neurons were largely uncorrelated. Additionally, vocalization-induced suppression was found to be preferentially distributed to upper cortical layers. Finally, we showed that the summation of all auditory cortical activity during vocalization, including both single and multi-unit responses, was weakly excitatory, consistent with observations from studies of the human brain during speech.

Pitch perception is crucial for vocal communication, music perception, and auditory object processing in a complex acoustic environment. The neural representation of pitch in the cerebral cortex has long been an outstanding question in auditory neuroscience. Several lines of evidence now point to a distinct non-primary region of auditory cortex in primates that contains a cortical representation of pitch.

No abstract

The ability to record well-isolated action potentials from individual neurons in naturally behaving animals is crucial for understanding neural mechanisms underlying natural behaviors. Traditional neurophysiology techniques, however, require the animal to be restrained which often restricts natural behavior. An example is the common marmoset (Callithrix jacchus), a highly vocal New World primate species, used in our laboratory to study the neural correlates of vocal production and sensory feedback. When restrained by traditional neurophysiological techniques marmoset vocal behavior is severely inhibited. Tethered recording systems, while proven effective in rodents pose limitations in arboreal animals such as the marmoset that typically roam in a three-dimensional environment. To overcome these obstacles, we have developed a wireless neural recording technique that is capable of collecting single-unit data from chronically implanted multi-electrodes in freely moving marmosets. A lightweight, low power and low noise wireless transmitter (headstage) is attached to a multi-electrode array placed in the premotor cortex of the marmoset. The wireless headstage is capable of transmitting 15 channels of neural data with signal-to-noise ratio (SNR) comparable to a tethered system. To minimize radio-frequency (RF) and electro-magnetic interference (EMI), the experiments were conducted within a custom designed RF/EMI and acoustically shielded chamber. The individual electrodes of the multi-electrode array were periodically advanced to densely sample the cortical layers. We recorded single-unit data over a period of several months from the frontal cortex of two marmosets. These recordings demonstrate the feasibility of using our wireless recording method to study single neuron activity in freely roaming primates.