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Auditory perception requires categorizing sound sequences, such as speech, into classes, such as syllables. Auditory categorization depends not only on the sequences’ acoustic waveform, but also on the listener’s sensory uncertainty, any individual sound’s relevance to the task, and learning the temporal statistics of the acoustic environment. However, whether and how these factors interact to shape categorization is unknown. Here, we measured human participants’ performance on a multi-tone categorization task. Task-relevant tones contributed more to category choice than task-irrelevant tones, confirming that participants combined information about sensory features with task relevance. Conversely, poor estimates of tones’ task relevance or high sensory uncertainty adversely impacted category choice. Learning temporal statistics of sound category also affected decisions. The magnitude of this effect correlated inversely with participants’ relevance estimates. These results demonstrate that humans differentially weigh sensory uncertainty, task relevance and learning, providing a novel understanding of sensory decision-making under real-life behavioral demands.

SummaryAlthough previous studies have identified neural mechanisms that may underlie auditory scene analysis, the relationship between these mechanisms and behavior remains elusive. To fill these gaps, we recorded multiunit activity (MUA) from the posterior and anterior auditory fields while monkeys participated in an auditory streaming task. We found that MUA magnitude was reduced as the streaming stimulus unfolded over time, and this reduction depended on the frequency difference between the tone bursts comprising the streaming stimulus. We then examined whether this frequency-dependent reduction in activity could be utilized by downstream neurons to read out “one stream” versus “two streams” and found that, as the frequency difference increased, an ideal observer consistently classified neural activity as “two streams”. However, because this classification was not modulated by the monkeys’ choices, it suggests that this activity may not reflect the segregation of stimuli into perceptually distinct auditory streams but may simply reflect bottom-up processes.

A fundamental scientific goal in auditory neuroscience is identifying what mechanisms allow the brain to transform an unlabeled mixture of auditory stimuli into distinct perceptual representations. This transformation is accomplished by a complex interaction of multiple neurocomputational processes, including Gestalt grouping mechanisms, categorization, attention, and perceptual decision-making. Despite a great deal of scientific energy devoted to understanding these principles of hearing, we still do not understand either how auditory perception arises from neural activity or the causal relationship between neural activity and auditory perception. Here, we review the contributions of cortical and subcortical regions to auditory perceptual decisions with an emphasis on those studies that simultaneously measure behavior and neural activity. We also put forth challenges to the field that must be faced if we are to further our understanding of the relationship between neural activity and auditory perception.

Expectations, such as those arising from either learned rules or recent stimulus regularities, can bias subsequent auditory perception in diverse ways. However, it is not well understood if and how these diverse effects depend on the source of the expectations. Further, it is unknown whether different sources of bias use the same or different computational and physiological mechanisms. We examined how rule-based and stimulus-based expectations influenced behavior and pupil- linked arousal, a marker of certain forms of expectation-based processing, of human subjects performing an auditory frequency-discrimination task. Rule-based cues consistently biased choices and response times (RTs) toward the more-probable stimulus. In contrast, stimulus-based cues had a complex combination of effects, including choice and RT biases toward and away from the frequency of recently presented stimuli. These different behavioral patterns also had: 1) distinct computational signatures, including different modulations of key components of a novel form of a drift-diffusion decision model and 2) distinct physiological signatures, including substantial bias- dependent modulations of pupil size in response to rule-based but not stimulus-based cues. These results imply that different sources of expectations can modulate auditory processing via distinct mechanisms: one that uses arousal-linked, rule-based information and another that uses arousal- independent, stimulus-based information to bias the speed and accuracy of auditory perceptual decisions.Author summaryPrior information about upcoming stimuli can bias our perception of those stimuli. Whether different sources of prior information bias perception in similar or distinct ways is not well understood. We compared the influence of two kinds of prior information on tone-frequency discrimination: rule-based cues, in the form of explicit information about the most-likely identity of the upcoming tone; and stimulus-based cues, in the form of sequences of tones presented before the to-be-discriminated tone. Although both types of prior information biased auditory decision- making, they demonstrated distinct behavioral, computational, and physiological signatures. Our results suggest that the brain processes prior information in a form-specific manner rather than utilizing a general-purpose prior. Such form-specific processing has implications for understanding decision biases real-world contexts, in which prior information comes from many different sources and modalities.

OBJECTIVE. A fundamental goal of the auditory system is to parse the auditory environment into distinct perceptual representations. Auditory perception is mediated by the ventral auditory pathway, which includes the ventrolateral prefrontal cortex (vlPFC). Because large-scale recordings of auditory signals are quite rare, the spatiotemporal resolution of the neuronal code that underlies vlPFC’s contribution to auditory perception has not been fully elucidated. Therefore, we developed a modular, chronic, high-resolution, multi-electrode array system with long-term viability in order to identify the information that could be decoded from μECoG vlPFC signals. APPROACH. We molded three separate μECoG arrays into one and implanted this system in a non-human primate. A custom 3D-printed titanium chamber was mounted on the left hemisphere. The molded 294-contact μECoG array was implanted subdurally over the vlPFC. μECoG activity was recorded while the monkey participated in a ‘hearing-in-noise’ task in which they reported hearing a ‘target’ vocalization from a background ‘chorus’ of vocalizations. We titrated task difficulty by varying the sound level of the target vocalization, relative to the chorus (target-to-chorus ratio, TCr). MAIN RESULTS. We decoded the TCr and the monkey’s behavioral choices from the μECoG signal. We analyzed decoding accuracy as a function of number of electrodes, spatial resolution, and time from implantation. Over a one-year period, we found significant decoding with individual electrodes that increased significantly as we decoded simultaneously more electrodes. Further, we found that the decoding for behavioral choice was better than the decoding of TCr. Finally, because the decoding accuracy of individual electrodes varied on a day-by-day basis, electrode arrays with high channel counts ensure robust decoding in the long term. SIGNIFICANCE. Our results demonstrate the utility of high-resolution and high-channel-count, chronic μECoG recording. We developed a surface electrode array that can be scaled to cover larger cortical areas without increasing the chamber footprint.

The brain parses the auditory environment into distinct sounds by identifying those acoustic features in the environment that have common relationships (e.g., spectral regularities) with one another and then grouping together the neuronal representations of these features. Although there is a large literature that tests how the brain tracks spectral regularities that are predictable, it is not known how the auditory system tracks spectral regularities that are not predictable and that change dynamically over time. Furthermore, the contribution of brain regions downstream of the auditory cortex to the coding of spectral regularity is unknown. Here, we addressed these two issues by recording electrocorticographic activity, while human patients listened to tone-burst sequences with dynamically varying spectral regularities, and identified potential neuronal mechanisms of the analysis of spectral regularities throughout the brain. We found that the degree of oscillatory stimulus phase consistency (PC) in multiple neuronal-frequency bands tracked spectral regularity. In particular, PC in the delta-frequency band seemed to be the best indicator of spectral regularity. We also found that these regularity representations existed in multiple regions throughout cortex. This widespread reliable modulation in PC – both in neuronal-frequency space and in cortical space – suggests that phase-based modulations may be a general mechanism for tracking regularity in the auditory system specifically and other sensory systems more generally. Our findings also support a general role for the delta-frequency band in processing the regularity of auditory stimuli.

A fundamental problem in hearing is detecting a “target” stimulus (e.g., a friend’s voice) that is presented with a noisy background (e.g., the din of a crowded restaurant). Despite its importance to hearing, a relationship between spiking activity and behavioral performance during such a “detection-in-noise” task has yet to be fully elucidated. In this study, we recorded spiking activity in primary auditory cortex (A1) while rhesus monkeys detected a target stimulus that was presented with a noise background. Although some neurons were modulated, the response of the typical A1 neuron was not modulated by the stimulus- and task-related parameters of our task. In contrast, we found more robust representations of these parameters in population-level activity: small populations of neurons matched the monkeys’ behavioral sensitivity. Overall, these findings are consistent with the hypothesis that the sensory evidence, which is needed to solve such detection-in-noise tasks, is represented in population-level A1 activity and may be available to be read out by downstream neurons that are involved in mediating this task. NEW & NOTEWORTHY This study examines the contribution of A1 to detecting a sound that is presented with a noisy background. We found that population-level A1 activity, but not single neurons, could provide the evidence needed to make this perceptual decision.

OBJECTIVEA fundamental goal of the auditory system is to parse the auditory environment into distinct perceptual representations. Auditory perception is mediated by the ventral auditory pathway, which includes the ventrolateral prefrontal cortex (vlPFC) late. Because large-scale recordings of auditory signals are quite rare, the spatiotemporal resolution of the neuronal code that underlies vlPFC’s contribution to auditory perception has not been fully elucidated. Therefore, we developed a modular, chronic, high-resolution, multi-electrode array system with long-term viability.APPROACHWe molded three separate μECoG arrays into one and implanted this system in a non-human primate. A custom 3D-printed titanium chamber was mounted on left hemisphere. The molded 294-contact μECoG array was implanted subdurally over vlPFC. μECoG activity was recorded while the monkey participated in a “hearing-in-noise” task in which they reported hearing a “target” vocalization from a background “chorus” of vocalizations. We titrated task difficulty by varying the sound level of the target vocalization, relative to the chorus (target-to-chorus ratio, TCr).MAIN RESULTSWe decoded the TCr and the monkey’s behavioral choices from the μECoG signal. We analyzed decoding capacity as a function of neuronal frequency band, spatial resolution, and time from implantation. Over a one-year period, we were successfully able to record μECoG signals. Although we found significant decoding with as few as two electrodes, we found near-perfect decoding with ∼16 electrodes. Decoding further improved when we included more electrodes. Finally, because the decoding capacity of individual electrodes varied on a day-by-day basis, high-density electrode arrays ensure robust decoding in the long term.SIGNIFICANCEOur results demonstrate the utility and robustness of high-resolution chronic µECoG recording. We developed a new high-resolution surface electrode array that can be scaled to cover larger cortical areas without increasing the chamber footprint.

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.

The intrinsic uncertainty of sensory information (i.e., evidence) does not necessarily deter an observer from making a reliable decision. Indeed, uncertainty can be reduced by integrating (accumulating) incoming sensory evidence. It is widely thought that this accumulation is instantiated via recurrent rate-code neural networks. Yet, these networks do not fully explain important aspects of perceptual decision-making, such as a subject’s ability to retain accumulated evidence during temporal gaps in the sensory evidence. Here, we utilized computational models to show that cortical circuits can switch flexibly between ‘retention’ and ‘integration’ modes during perceptual decision-making. Further, we found that, depending on how the sensory evidence was readout, we could simulate ‘stepping’ and ‘ramping’ activity patterns, which may be analogous to those seen in different studies of decision-making in the primate parietal cortex. This finding may reconcile these previous empirical studies because it suggests these two activity patterns emerge from the same mechanism.

Our understanding of the large-scale population dynamics of neural activity is limited, in part, by our inability to record simultaneously from large regions of the cortex. Here, we validated the use of a large-scale active microelectrode array that simultaneously records 196 multiplexed micro-electrocortigraphical (μECoG) signals from the cortical surface at a very high density (1,600 electrodes/cm2). We compared μECoG measurements in auditory cortex using a custom “active” electrode array to those recorded using a conventional “passive” μECoG array. Both of these array responses were also compared with data recorded via intrinsic optical imaging, which is a standard methodology for recording sound-evoked cortical activity. Custom active μECoG arrays generated more veridical representations of the tonotopic organization of the auditory cortex than current commercially available passive μECoG arrays. Furthermore, the cortical representation could be measured efficiently with the active arrays, requiring as little as 13.5 s of neural data acquisition. Next, we generated spectrotemporal receptive fields from the recorded neural activity on the active μECoG array and identified functional organizational principles comparable to those observed using intrinsic metabolic imaging and single-neuron recordings. This new electrode array technology has the potential for large-scale, temporally precise monitoring and mapping of the cortex, without the use of invasive penetrating electrodes.

A listener’s capacity to discriminate between sounds is related to the amount of acoustic variability that exists between these sounds. However, a full understanding of how this natural variability impacts neural activity and behavior is lacking. Here, we tested monkeys’ ability to discriminate between different utterances of vocalizations from the same acoustic class (i.e., coos and grunts), while neural activity was simultaneously recorded in the anterolateral belt region (AL) of the auditory cortex, a brain region that is a part of a pathway that mediates auditory perception. Monkeys could discriminate between coos better than they could discriminate between grunts. We also found AL activity was more informative about different coos than different grunts. This difference could be attributed, in part, to our finding that coos had more acoustic variability than grunts. Thus, intrinsic acoustic variability constrained the discriminability of AL spike trains and the ability of rhesus monkeys to discriminate between vocalizations.

Acoustic communication between animals requires them to detect, discriminate, and categorize conspecific or heterospecific vocalizations in their natural environment. Laboratory studies of the auditory-processing abilities that facilitate these tasks have typically employed a broad range of acoustic stimuli, ranging from natural sounds like vocalizations to "artificial" sounds like pure tones and noise bursts. However, even when using vocalizations, laboratory studies often test abilities like categorization in relatively artificial contexts. Consequently, it is not clear whether neural and behavioral correlates of these tasks (1) reflect extensive operant training, which drives plastic changes in auditory pathways, or (2) the innate capacity of the animal and its auditory system. Here, we review a number of recent studies, which suggest that adopting more ethological paradigms utilizing natural communication contexts are scientifically important for elucidating how the auditory system normally processes and learns communication sounds. Additionally, since learning the meaning of communication sounds generally involves social interactions that engage neuromodulatory systems differently than laboratory-based conditioning paradigms, we argue that scientists need to pursue more ethological approaches to more fully inform our understanding of how the auditory system is engaged during acoustic communication. This article is part of a Special Issue entitled "Communication Sounds and the Brain: New Directions and Perspectives".

Communication signals in nonhuman primates are inherently multimodal. However, for laboratory-housed monkeys, there is relatively little evidence in support of the use of multimodal communication signals in individual recognition. Here, we used a preferential-looking paradigm to test whether laboratory-housed rhesus monkeys could ‘spontaneously' (i.e., in the absence of operant training) use multimodal communication stimuli to discriminate between known conspecifics. The multimodal stimulus was a silent movie of 2 monkeys vocalizing and an audio file of the vocalization from one of the monkeys in the movie. We found that the gaze patterns of the monkeys that knew the individuals in the movie were reliably biased toward the individual that did not produce the vocalization. In contrast, there was not a systematic gaze pattern for the monkeys that did not know the individuals in the movie. These data are consistent with the hypothesis that laboratory-housed rhesus macaques can recognize and distinguish between conspecifics based on auditory and visual communication signals.

Local field potentials (LFPs) and spiking activity reflect different types of information procssing. For example, neurophysiological studies indicate that signal novelty in the ventrolateral prefrontal cortex is differentially represented by LFPs and spiking activity: LFPs habituate to repeated stimulus presentations, whereas spiking activity does not. The neural mechanisms that allow for this differential representation between LFPs and spiking activity are not clear. Here, we model and simulate LFPs and spiking activity of neurons in the ventrolateral prefrontal cortex in order to elucidate potential mechanisms underlying this differential representation. We demonstrate that dynamic negative-feedback loops cause LFPs to habituate in response to repeated presentations of the same stimulus while spiking activity is maintained. This disassociation between LFPs and spiking activity may be a mechanism by which LFPs code stimulus novelty, whereas spiking activity carries abstract information, such as category membership and decision-related activity.

The fundamental problem in audition is determining the mechanisms required by the brain to transform an unlabelled mixture of auditory stimuli into coherent perceptual representations. This process is called auditory-scene analysis. The perceptual representations that result from auditory-scene analysis are formed through a complex interaction of perceptual grouping, attention, categorization and decision-making. Despite a great deal of scientific energy devoted to understanding these aspects of hearing, we still do not understand (1) how sound perception arises from neural activity and (2) the causal relationship between neural activity and sound perception. Here, we review the role of the “ventral” auditory pathway in sound perception. We hypothesize that, in the early parts of the auditory cortex, neural activity reflects the auditory properties of a stimulus. However, in latter parts of the auditory cortex, neurons encode the sensory evidence that forms an auditory decision and are causally involved in the decision process. Finally, in the prefrontal cortex, which receives input from the auditory cortex, neural activity reflects the actual perceptual decision. Together, these studies indicate that the ventral pathway contains hierarchical circuits that are specialized for auditory perception and scene analysis.

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.

Over a decade ago it was proposed that the primate auditory cortex is organized in a serial and parallel manner in which there is a dorsal stream processing spatial information and a ventral stream processing non-spatial information. This organization is similar to the “what”/“where” processing of the primate visual cortex. This review will examine several key studies, primarily electrophysiological, that have tested this hypothesis. We also review several human imaging studies that have attempted to define these processing streams in the human auditory cortex. While there is good evidence that spatial information is processed along a particular series of cortical areas, the support for a non-spatial processing stream is not as strong. Why this should be the case and how to better test this hypothesis is also discussed.

Goal-directed behavior can be thought of as dynamic links between sensory stimuli and motor acts. Neural correlates of many of the intermediate events of both auditory and visual goal-directed behaviors are found in the posterior parietal cortex. Here, we review studies that have focused on how neurons in the lateral intraparietal area (area LIP) differentially process auditory and visual stimuli. Together, these studies suggest that area LIP contains a modality-dependent representation that is highly dependent on behavioral context.

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.

Summary 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.

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 can be characterized as a dynamic link between a sensory stimulus and a motor act. Neural correlates of many of the intermediate events of goal-directed behavior are found in the posterior parietal cortex. Although the parietal cortex’s role in guiding visual behaviors has received considerable attention, relatively little is known about its role in mediating auditory behaviors. Here, the authors review recent studies that have focused on how neurons in the lateral intraparietal area (area LIP) differentially process auditory and visual stimuli. These studies suggest that area LIP contains a modality-dependent representation that is highly dependent on behavioral context.

We tested the responses of neurons in the lateral parietal area (area LIP) for their sensitivity to the spatial and non-spatial attributes of an auditory stimulus. We found that the firing rates of LIP neurons were modulated by both of these attributes. These data indicate that, while area LIP is involved in spatial processing, non-spatial processing is not restricted to independent channels.

Spatial and nonspatial auditory processing is hypothesized to occur in parallel dorsal and ventral pathways, respectively. In this study, we tested the spatial and nonspatial sensitivity of auditory neurons in the ventrolateral prefrontal cortex (vPFC), a cortical area in the hypothetical nonspatial pathway. We found that vPFC neurons were modulated significantly by both the spatial and nonspatial attributes of an auditory stimulus. When comparing these responses with those in anterolateral belt region of the auditory cortex, which is hypothesized to be specialized for processing the nonspatial attributes of auditory stimuli, we found that the nonspatial sensitivity of vPFC neurons was poorer, whereas the spatial selectivity was better than anterolateral neurons. Also, the spatial and nonspatial sensitivity of vPFC neurons was comparable with that seen in the lateral intraparietal area, a cortical area that is a part of the dorsal pathway. These data suggest that substantial spatial and nonspatial processing occurs in both the dorsal and ventral pathways.

Auditory spatial information arises in a head-centered coordinate frame, whereas the saccade command signals generated by the superior colliculus (SC) are thought to specify target locations in an eye-centered frame. However, auditory activity in the SC appears to be neither head- nor eye-centered but in a reference frame that is intermediate between both of these reference frames. This neurophysiological finding suggests that auditory saccades might not fully compensate for changes in initial eye position. Here, we investigated whether the accuracy of saccades to sounds is affected by initial eye position in rhesus monkeys. We found that, on average, a 12° horizontal shift in initial eye position produced only a 0.6 to 1.6° horizontal shift in the endpoints of auditory saccades made to targets at a range of locations along the horizontal meridian. This shift was similar in size to the modest influence of eye position on visual saccades. This virtually complete compensation for initial eye position implies that auditory activity in the SC is read out in a manner that is appropriate for generating accurate saccades to sounds.

Prior to examining the neural correlates of auditory cognition with ethologically relevant stimuli, it is first necessary to establish that laboratory-housed animals respond to these stimuli with species-typical responses. Here, we report the results of experiments on laboratory-housed rhesus monkeys using both species-typical vocalizations and band-pass noise. Paralleling the approach used in field studies of this species, we used a habituation-discrimination paradigm in which auditory stimuli were presented and a monkey’s orienting responses to the stimuli were quantified. In parallel with the results obtained in field studies, we found that laboratory-housed rhesus classified species-typical vocalizations according to their putative referent properties as opposed to similarities in their acoustic morphology. In control experiments, monkeys oriented to band-pass noise but did not categorize differences in the spectral composition of the noise stimuli. These findings support the hypothesis that laboratory-housed rhesus classify, in the absence of training, species-typical vocalizations in a manner comparable to rhesus monkeys living under more natural conditions. As such, species-typical vocalizations are an appropriate and necessary class of stimuli in experiments that explore the neural correlates of auditory cognition in rhesus monkeys from a neuroethological perspective.

We examined the responses of neurons in the parietal reach region (PRR) during reaches to the remembered locations of auditory or visual stimuli. We found that the firing rate of PRR neurons contained information about the location of auditory and visual stimuli. For neurons tested with visual stimuli, the amount of information remained constant throughout the task. In contrast, for neurons tested with auditory stimuli, the amount of target-location information increased as the trial evolved. During the reach period of the task, the amount of information that was carried by neurons tested with auditory stimuli was not statistically different from the amount carried by neurons tested with visual stimuli. We interpret these data to suggest that the type of information that PRR neurons encode evolves throughout a task.

The auditory system determines the location of stimuli based on the evaluation of specific cues. The analysis begins in the tonotopic pathway, where these cues are processed in parallel, frequency-specific channels. This frequency-specific information is processed further in the midbrain and in the forebrain by specialized, space-processing pathways that integrate information across frequency channels, creating high-order neurons tuned to specific locations in space. Remarkably, the results of this integrative step are represented very differently in the midbrain and forebrain: in the midbrain, space is represented in maps, whereas, in the forebrain, space is represented in clusters of similarly tuned neurons. We propose that these different representations reflect the different roles that these two brain areas have in guiding behavior.

Cohen, Yale E. and Eric I. Knudsen. Representation of binaural spatial cues in Field L of the barn owl forebrain. J. Neurophysiol. 79: 879–890, 1998. This study examined the representation of spatial information in the barn owl Field L, the first telencephalic processing stage of the classical auditory pathway. Field L units were recorded extracellularly, and their responses to dichotically presented interaural time differences (ITD) and interaural level differences (ILD) were tested. We observed a variety of tuning profiles in Field L. Some sites were not sensitive to ITD or ILD. Other sites, especially those in the high-frequency region, were highly selective for values of ITD and ILD. These sites had multipeaked (commonly called “phase ambiguous”) ITD tuning profiles and were tuned for a single value of ILD. The tuning properties of these sites are similar to those seen in the lateral shell of the central nucleus of the inferior colliculus. Although the tuning properties of Field L sites were similar to those observed in the inferior colliculus, the functional organization of this spatial information was fundamentally different. Whereas in the inferior colliculus spatial information is organized into global topographics maps, in Field L spatial information is organized into local clusters, with sites having similar binaural tuning properties grouped together. The representation of binaural cues in Field L suggests that it is involved in auditory space processing but at a lower level of information processing than the auditory archistriatum, a forebrain area that is specialized for processing spatial information, and that the levels of information processing in the forebrain space processing pathway are remarkably similar to those in the well-known midbrain space processing pathway.

Cohen, Yale E., Greg L. Miller, and Eric I. Knudsen. Forebrain pathway for auditory space processing in the barn owl. J. Neurophysiol. 79: 891–902, 1998. The forebrain plays an important role in many aspects of sound localization behavior. Yet, the forebrain pathway that processes auditory spatial information is not known for any species. Using standard anatomic labeling techniques, we used a “top-down” approach to trace the flow of auditory spatial information from an output area of the forebrain sound localization pathway (the auditory archistriatum, AAr), back through the forebrain, and into the auditory midbrain. Previous work has demonstrated that AAr units are specialized for auditory space processing. The results presented here show that the AAr receives afferent input from Field L both directly and indirectly via the caudolateral neostriatum. Afferent input to Field L originates mainly in the auditory thalamus, nucleus ovoidalis, which, in turn, receives input from the central nucleus of the inferior colliculus. In addition, we confirmed previously reported projections of the AAr to the basal ganglia, the external nucleus of the inferior colliculus (ICX), the deep layers of the optic tectum, and various brain stem nuclei. A series of inactivation experiments demonstrated that the sharp tuning of AAr sites for binaural spatial cues depends on Field L input but not on input from the auditory space map in the midbrain ICX: pharmacological inactivation of Field L eliminated completelyauditory responses in the AAr, whereas bilateral ablation of the midbrain ICX had no appreciable effect on AAr responses. We conclude, therefore, that the forebrain sound localization pathway can process auditory spatial information independently of the midbrain localization pathway.

The present investigation considered the effects of cochlear damage caused by exposure to intense sound on the nucleus magnocellularis of the chick. Neonatal chicks exposed to intense sound were separated into four groups with post-exposure recovery durations of 0, 15, 27, and 43 days. Four age-matched, non-exposed control groups were also formed. At each recovery interval, the control and exposed birds were sacrificed and their brains prepared for paraffin embedding. The brain stem region containing the nucleus magnocellularis (NM) was serially sectioned in the coronal plane. All sections containing NM cells were identified and then coded in terms of their percentile distance from the most caudolateral section. Sections along the nucleus at the 15th, 30th, 50th, 65th, 80th, and 95th percentile positions were selected for evaluation, and the cross-sectional areas of individual NM cells in these sections were then measured. Cell areas were corrected for the bias introduced by eccentricity of the nucleus. The number of NM cells per 1,000 μm2 was also calculated at the 50th and 65th percentile positions. These procedures were repeated for the age-matched, non-exposed control animals. The cross-sectional cell area in exposed animals, immediately after the exposure, was reduced significantly at all positions, but returned to near normal by 43 days of recovery. However, the coronal area of NM in the sections at the 50th and 65th percentile position, as well as NM cell density, were unaffected by the exposure at all recovery intervals. The observation of structural recovery in NM cells at 43 days post-exposure was remarkable because it occurred at least 4 weeks after complete functional restoration of single-cell activity in the NM. The shrinkage in NM cell size throughout the nucleus may be due to a general reduction in spontaneous activity in the cochlear nerve fibers caused by the acoustic injury to the chick basilar papilla. J. Comp. Neurol. 390:412–426, 1998. © 1998 Wiley-Liss, Inc.

Perceptual representations of auditory stimuli (i.e., sounds) are derived from the auditory system's ability to segregate and group the spectral, temporal, and spatial features of auditory stimuli—a process called “auditory scene analysis”. Psychophysical studies have identified several of the principles and mechanisms that underlie a listener's ability to segregate and group acoustic stimuli. One important psychophysical task that has illuminated many of these principles and mechanisms is the “streaming” task. Despite the wide use of this task to study psychophysical mechanisms of human audition, no studies have explicitly tested the streaming abilities of non-human animals using the standard methodologies employed in human-audition studies. Here, we trained rhesus macaques to participate in the streaming task using methodologies and controls similar to those presented in previous human studies. Overall, we found that the monkeys' behavioral reports were qualitatively consistent with those of human listeners, thus suggesting that this task may be a valuable tool for future neurophysiological studies.