Faculty Bibliography

Spatial and non-spatial sensory information is hypothesized to be evaluated in parallel pathways. In this study, we tested the spatial and non-spatial sensitivity of auditory neurons in the ventrolateral prefrontal cortex (vPFC), a cortical area in the non-spatial pathway. Activity was tested while non-human primates reported changes in an auditory stimulus' spatial or non-spatial features. We found that vPFC neurons were reliably modulated during a non-spatial auditory task but were not modulated during a spatial auditory task. The degree of modulation during the non-spatial task correlated positively with the monkeys' behavioral performance. These results are consistent with the hypotheses that the vPFC is part of a circuit involved in non-spatial auditory processing and that the vPFC plays a functional role in non-spatial auditory cognition.

Adaptive behavior requires that animals integrate current and past information with their decision-making. One important type of information is auditory-communication signals (i.e., species-specific vocalizations). Here, we tested how rhesus monkeys incorporate the opportunity to listen to different species-specific vocalizations into their decision-making processes. In particular, we tested how monkeys value these vocalizations relative to the opportunity to get a juice reward. To test this hypothesis, monkeys chose one of two targets to get a varying juice reward; at one of those targets, in addition to the juice reward, a vocalization was presented. By titrating the juice amounts at the two targets, we quantified the relationship between the monkeys' juice choices relative to the opportunity to listen to a vocalization. We found that, rhesus were not willing to give up a large juice reward to listen to vocalizations indicating that, relative to a juice reward, listening to vocalizations has a low value.

The neural correlates that relate auditory categorization to aspects of goal-directed behavior, such as decision-making, are not well understood. Since the prefrontal cortex (PFC) plays an important role in executive function and the categorization of auditory objects, we hypothesized that neural activity in the PFC should predict an animal's behavioral reports (decisions) during a category task. To test this hypothesis, we tested PFC activity that was recorded while monkeys categorized human spoken words (Russ et al., 2008b). We found that activity in the ventrolateral PFC, on average, correlated best with the monkeys' choices than with the auditory stimuli. This finding demonstrates a direct link between PFC activity and behavioral choices during a non-spatial auditory task.

The detection of stimuli is critical for an animal's survival [1]. However, it is not adaptive for an animal to respond automatically to every stimulus that is present in the environment [2-5]. Given that the prefrontal cortex (PFC) plays a key role in executive function [6-8], we hypothesized that PFC activity should be involved in context-dependent responses to uncommon stimuli. As a test of this hypothesis, monkeys participated in a same-different task, a variant of an oddball task [2]. During this task, a monkey heard multiple presentations of a "reference" stimulus that were followed by a "test" stimulus and reported whether these stimuli were the same or different. While they participated in this task, we recorded from neurons in the ventrolateral prefrontal cortex (vPFC; a cortical area involved in aspects of nonspatial auditory processing [9, 10]). We found that vPFC activity was correlated with the monkeys' choices. This finding demonstrates a direct link between single neurons and behavioral choices in the PFC on a nonspatial auditory task.

The neural computations that underlie the processing of auditory-stimulus identity are not well understood, especially how information is transformed across different cortical areas. Here, we compared the capacity of neurons in the superior temporal gyrus (STG) and the ventrolateral prefrontal cortex (vPFC) to code the identity of an auditory stimulus; these two areas are part of a ventral processing stream for auditory-stimulus identity. Whereas the responses of neurons in both areas are reliably modulated by different vocalizations, STG responses code significantly more vocalizations than those in the vPFC. Together, these data indicate that the STG and vPFC differentially code auditory identity, which suggests that substantial information processing takes place between these two areas. These findings are consistent with the hypothesis that the STG and the vPFC are part of a functional circuit for auditory-identity analysis.

Goal-directed behavior is the essence of adaptation because it allows humans and other animals to respond dynamically to different environmental scenarios. Goal-directed behavior can be characterized as the formation of dynamic links between stimuli and actions. One important attribute of goal-directed behavior is that linkages can be formed based on how a stimulus is categorized. That is, links are formed based on the membership of a stimulus in a particular functional category. In this review, we review categorization with an emphasis on auditory categorization. We focus on the role of categorization in language and non-human vocalizations. We present behavioral data indicating that non-human primates categorize and respond to vocalizations based on differences in their putative meaning and not differences in their acoustics. Finally, we present evidence suggesting that the ventrolateral prefrontal cortex plays an important role in processing auditory objects and has a specific role in the representation of auditory categories.

Communication is one of the fundamental components of both human and nonhuman animal behavior. Auditory communication signals (i.e., vocalizations) are especially important in the socioecology of several species of nonhuman primates such as rhesus monkeys. In rhesus, the ventrolateral prefrontal cortex (vPFC) is thought to be part of a circuit involved in representing vocalizations and other auditory objects. To further our understanding of the role of the vPFC in processing vocalizations, we characterized the spectrotemporal features of rhesus vocalizations, compared these features with other classes of natural stimuli, and then related the rhesus-vocalization acoustic features to neural activity. We found that the range of these spectrotemporal features was similar to that found in other ensembles of natural stimuli, including human speech, and identified the subspace of these features that would be particularly informative to discriminate between different vocalizations. In a first neural study, however, we found that the tuning properties of vPFC neurons did not emphasize these particularly informative spectrotemporal features. In a second neural study, we found that a first-order linear model (the spectrotemporal receptive field) is not a good predictor of vPFC activity. The results of these two neural studies are consistent with the hypothesis that the vPFC is not involved in coding the first-order acoustic properties of a stimulus but is involved in processing the higher-order information needed to form representations of auditory objects.

Goal-directed behavior is characterized by flexible stimulus-action mappings. The lateral intraparietal area (area LIP) contains a representation of extra-personal space that is used to guide goal-directed behavior. To examine further how area LIP contributes to these flexible stimulus-action mappings, we recorded LIP activity while rhesus monkeys participated in two different cueing tasks. In the first task, the color of a central light indicated the location of a monkey's saccadic endpoint in the absence of any other visual stimuli. In the second task, the color of a central light indicated which of two visual targets was the saccadic goal. In both tasks, LIP activity was modulated by these non-spatial cues. These observations further suggest a role for area LIP in mediating endogenous associations that link stimuli with actions.

In various aspects of linguistic analysis and human cognition, some forms of observed variation are ignored in the service of handling more abstract categories. In the absence of training, rhesus discriminate between different types of vocalizations based on the information conveyed as opposed to their acoustic morphologies. We hypothesized that neurons in the ventrolateral prefrontal cortex (vPFC), an area involved in auditory-object processing, might be involved in this spontaneous categorization. To test this hypothesis, we recorded vPFC activity while rhesus listened to vocalizations conveying information about food and non-food events. Results showed between, but not within category discrimination. That is, vPFC neurons discriminated between vocalizations associated with food versus non-food events but not within the class of food calls associated with differences in quality. These results indicate that the vPFC plays a significant role in spontaneously processing abstract categorical information.