Auditory perceptual decisions are thought to be mediated by the ventral auditory pathway. However, the specific and causal contributions of different brain regions in this pathway, including the middle-lateral (ML) and anterolateral (AL) belt regions of the auditory cortex, to auditory decisions have not been fully identified. To identify these contributions, we recorded from and microstimulated ML and AL sites while monkeys decided whether an auditory stimulus contained more low-frequency or high-frequency tone bursts. Both ML and AL neural activity was modulated by the frequency content of the stimulus. However, only the responses of the most stimulus-sensitive AL neurons were systematically modulated by the monkeys’ choices. Consistent with this observation, microstimulation of AL—but not ML—systematically biased the monkeys’ behavior toward the choice associated with the preferred frequency of the stimulated site. Together, these findings suggest that AL directly and causally contributes sensory evidence used to form this auditory decision.

Tsunada J, Lee JH, Cohen YE. Representation of speech categories in the primate auditory cortex.

Vocal communication is a sensory-motor process requiring auditory self-monitoring to correct errors and to ensure accurate vocal production. When presented with altered speech feedback, humans rapidly change their speech to compensate. Although previous evidence has demonstrated suppression of auditory cortex during both speech and animal vocalization, the specific role of auditory cortex in such feedback-dependent control is unknown. Here we show the relationship between neural activity in the auditory cortex and feedback-dependent vocal control in marmoset monkeys. We demonstrate that marmosets, like humans, exhibit feedback control of vocal acoustics. We further show that feedback-sensitive activity of auditory cortex neurons predict such compensatory vocal changes. Finally, we demonstrate that electrical microstimulation of auditory cortex rapidly evokes similar changes in vocal production. These results are evidence for a causal role of auditory cortex in vocal self-monitoring and feedback-dependent control, and have implications for understanding human speech motor control.

Key points• The role that pyramidal neurons and interneurons have in auditory behaviour and cognition remains unknown.• In this study, we tested the hypothesis that pyramidal cells and interneurons in the auditory cortex play a differential role in auditory categorization.• Putative interneurons in the auditory cortex were more selective for auditory categories than putative pyramidal neurons.• The greater category selectivity in putative interneurons may be a characteristic of auditory categorization in the microcircuit of the auditory cortex.Abstract A comprehensive understanding of the neural mechanisms of cognitive function requires an understanding of how neural representations are transformed across different scales of neural organization: from within local microcircuits to across different brain areas. However, the neural transformations within the local microcircuits are poorly understood. Particularly, the role that two main cell classes of neurons in cortical microcircuits (i.e. pyramidal neurons and interneurons) have in auditory behaviour and cognition remains unknown. In this study, we tested the hypothesis that pyramidal cells and interneurons in the auditory cortex play a differential role in auditory categorization. To test this hypothesis, we recorded single-unit activity from the auditory cortex of rhesus monkeys while they categorized speech sounds. Based on the spike-waveform shape, a neuron was classified as either a narrow-spiking putative interneuron or a broad-spiking putative pyramidal neuron. We found that putative interneurons and pyramidal neurons in the auditory cortex differentially coded category information: interneurons were more selective for auditory categories than pyramidal neurons. These differences between cell classes may be an essential property of the neural computations underlying auditory categorization within the microcircuitry of the auditory cortex.

The advent of cranial implants revolutionized primate neurophysiological research because they allow researchers to stably record neural activity from monkeys during active behavior. Cranial implants have improved over the years since their introduction, but chronic implants still increase the risk for medical complications including bacterial contamination and resultant infection, chronic inflammation, bone and tissue loss and complications related to the use of dental acrylic. These complications can lead to implant failure and early termination of study protocols. In an effort to reduce complications, we describe several refinements that have helped us improve cranial implants and the wellbeing of implanted primates.

Categorization enables listeners to efficiently encode and respond to auditory stimuli. Behavioral evidence for auditory categorization has been well documented across a broad range of human and non-human animal species. Moreover, neural correlates of auditory categorization have been documented in a variety of different brain regions in the ventral auditory pathway, which is thought to underlie auditory-object processing and auditory perception. Here, we review and discuss how neural representations of auditory categories are transformed across different scales of neural organization in the ventral auditory pathway: from across different brain areas to within local microcircuits. We propose different neural transformations across different scales of neural organization in auditory categorization. Along the ascending auditory system in the ventral pathway, there is a progression in the encoding of categories from simple acoustic categories to categories for abstract information. On the other hand, in local microcircuits, different classes of neurons differentially compute categorical information.

Perceptual decisions do not occur in isolation but instead reflect ongoing evaluation and adjustment processes that can affect future decisions. However, the neuronal substrates of these across-decision processes are not well understood, particularly for auditory decisions. We measured and manipulated the activity of choice-selective neurons in the ventrolateral prefrontal cortex (vlPFC) while monkeys made decisions about the frequency content of noisy auditory stimuli. As the decision was being formed, vlPFC activity was not modulated strongly by the task. However, after decision commitment, vlPFC population activity encoded the sensory evidence, choice, and outcome of the current trial and predicted subject-specific choice biases on the subsequent trial. Consistent with these patterns of neuronal activity, electrical microstimulation in vlPFC tended to affect the subsequent, but not current, decision. Thus, distributed post-commitment representations of graded decision-related information in prefrontal cortex can play a causal role in evaluating past decisions and biasing subsequent ones.

Vocal production is a sensory-motor process in which auditory self-monitoring is used to ensure accurate communication. During vocal production, the auditory cortex of both humans and animals is suppressed, a phenomenon that plays an important role in self-monitoring and vocal motor control. However, the underlying neural mechanisms of this vocalizationinduced suppression are unknown. c-band oscillations (.25 Hz) have been implicated a variety of cortical functions and are thought to arise from activity of local inhibitory interneurons, but have not been studied during vocal production. We therefore examined c-band activity in the auditory cortex of vocalizing marmoset monkeys, of either sex, and found that c responses increased during vocal production. This increase in c contrasts with simultaneously recorded suppression of singleunit and multiunit responses. Recorded vocal c oscillations exhibited two separable components: a vocalization-specific nonsynchronized ("induced") response correlating with vocal suppression, and a synchronized ("evoked") response that was also present during passive sound playback. These results provide evidence for the role of cortical c oscillations during inhibitory processing. Furthermore, the two distinct components of the c response suggest possible mechanisms for vocalization-induced suppression, and may correspond to the sensory-motor integration of top-down and bottom-up inputs to the auditory cortex during vocal production.