Gradient boosted decision trees reveal nuances of auditory discrimination behavior.

Animal psychophysics can generate rich behavioral datasets, often comprised of many 1000s of trials for an individual subject. Gradient-boosted models are a promising machine learning approach for analyzing such data, partly due to the tools that allow users to gain insight into how the model makes predictions. We trained ferrets to report a target word's presence, timing, and lateralization within a stream of consecutively presented non-target words. To assess the animals' ability to generalize across pitch, we manipulated the fundamental frequency (F0) of the speech stimuli across trials, and to assess the contribution of pitch to streaming, we roved the F0 from word token to token. We then implemented gradient-boosted regression and decision trees on the trial outcome and reaction time data to understand the behavioral factors behind the ferrets' decision-making. We visualized model contributions by implementing SHAPs feature importance and partial dependency plots. While ferrets could accurately perform the task across all pitch-shifted conditions, our models reveal subtle effects of shifting F0 on performance, with within-trial pitch shifting elevating false alarms and extending reaction times. Our models identified a subset of non-target words that animals commonly false alarmed to. Follow-up analysis demonstrated that the spectrotemporal similarity of target and non-target words rather than similarity in duration or amplitude waveform was the strongest predictor of the likelihood of false alarming. Finally, we compared the results with those obtained with traditional mixed effects models, revealing equivalent or better performance for the gradient-boosted models over these approaches.

Dissociable Neural Correlates of Multisensory Coherence and Selective Attention.

Previous work has demonstrated that performance in an auditory selective attention task can be enhanced or impaired, depending on whether a task-irrelevant visual stimulus is temporally coherent with a target auditory stream or with a competing distractor. However, it remains unclear how audiovisual (AV) temporal coherence and auditory selective attention interact at the neurophysiological level. Here, we measured neural activity using EEG while human participants (men and women) performed an auditory selective attention task, detecting deviants in a target audio stream. The amplitude envelope of the two competing auditory streams changed independently, while the radius of a visual disk was manipulated to control the AV coherence. Analysis of the neural responses to the sound envelope demonstrated that auditory responses were enhanced largely independently of the attentional condition: both target and masker stream responses were enhanced when temporally coherent with the visual stimulus. In contrast, attention enhanced the event-related response evoked by the transient deviants, largely independently of AV coherence. These results provide evidence for dissociable neural signatures of bottom-up (coherence) and top-down (attention) effects in AV object formation.SIGNIFICANCE STATEMENT Temporal coherence between auditory stimuli and task-irrelevant visual stimuli can enhance behavioral performance in auditory selective attention tasks. However, how audiovisual temporal coherence and attention interact at the neural level has not been established. Here, we measured EEG during a behavioral task designed to independently manipulate audiovisual coherence and auditory selective attention. While some auditory features (sound envelope) could be coherent with visual stimuli, other features (timbre) were independent of visual stimuli. We find that audiovisual integration can be observed independently of attention for sound envelopes temporally coherent with visual stimuli, while the neural responses to unexpected timbre changes are most strongly modulated by attention. Our results provide evidence for dissociable neural mechanisms of bottom-up (coherence) and top-down (attention) effects on audiovisual object formation.

Reversible Inactivation of Ferret Auditory Cortex Impairs Spatial and Nonspatial Hearing.

A key question in auditory neuroscience is to what extent are brain regions functionally specialized for processing specific sound features, such as location and identity. In auditory cortex, correlations between neural activity and sounds support both the specialization of distinct cortical subfields, and encoding of multiple sound features within individual cortical areas. However, few studies have tested the contribution of auditory cortex to hearing in multiple contexts. Here we determined the role of ferret primary auditory cortex in both spatial and nonspatial hearing by reversibly inactivating the middle ectosylvian gyrus during behavior using cooling (n = 2 females) or optogenetics (n = 1 female). Optogenetic experiments used the mDLx promoter to express Channelrhodopsin-2 in GABAergic interneurons, and we confirmed both viral expression (n = 2 females) and light-driven suppression of spiking activity in auditory cortex, recorded using Neuropixels under anesthesia (n = 465 units from 2 additional untrained female ferrets). Cortical inactivation via cooling or optogenetics impaired vowel discrimination in colocated noise. Ferrets implanted with cooling loops were tested in additional conditions that revealed no deficit when identifying vowels in clean conditions, or when the temporally coincident vowel and noise were spatially separated by 180 degrees. These animals did, however, show impaired sound localization when inactivating the same auditory cortical region implicated in vowel discrimination in noise. Our results demonstrate that, as a brain region showing mixed selectivity for spatial and nonspatial features of sound, primary auditory cortex contributes to multiple forms of hearing.SIGNIFICANCE STATEMENT Neurons in primary auditory cortex are often sensitive to the location and identity of sounds. Here we inactivated auditory cortex during spatial and nonspatial listening tasks using cooling, or optogenetics. Auditory cortical inactivation impaired multiple behaviors, demonstrating a role in both the analysis of sound location and identity and confirming a functional contribution of mixed selectivity observed in neural activity. Parallel optogenetic experiments in two additional untrained ferrets linked behavior to physiology by demonstrating that expression of Channelrhodopsin-2 permitted rapid light-driven suppression of auditory cortical activity recorded under anesthesia.

Pet Owner Perception of Ferret Boredom and Consequences for Housing, Husbandry, and Environmental Enrichment.

Boredom is a potential chronic but overlooked animal welfare problem. Caused by monotony, sub-optimal stimulation, and restrictive housing, boredom can therefore affect companion animals, particularly those traditionally caged, such as ferrets. We surveyed owners' (n = 621) perceptions of ferrets' capacity to experience boredom, behaviours they associate with it, and whether their perception of their ferrets' capacity for boredom influenced training techniques, housing, and environmental enrichment (EE). Most (93.0%) owners believed that ferrets could experience boredom, but owners who doubted that ferrets experience boredom (7.0%) provided slightly but significantly fewer EE types to their ferrets. Heat map and classification tree analysis showed that owners identified scratching at enclosure walls (n = 420) and excessive sleeping (n = 312) as distinctive behavioural indicators of ferret boredom. Repetitive pacing (n = 381), yawning (n = 191), and resting with eyes open (n = 171) were also suggested to indicate ferret boredom, but these overlapped with other states. Finally, ferret owners suggested social housing, tactile interaction with humans, and exploration as most important for preventing boredom. These results suggest that pet ferrets are at risk of reduced welfare from owners who doubt they can experience boredom, highlighting an opportunity to improve welfare through information dissemination. We recommend further investigation into ferret boredom capacity, behavioural indicators, and mitigation strategies.

Correction: Dancer et al. Housing and Environmental Enrichment of the Domestic Ferret: A Multi-Sector Survey. Animals 2022, 12, 1065.

There was an error in the original publication [...].

Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility.

Theta oscillations are a hallmark of hippocampal activity across mammals and play a critical role in many hippocampal models of memory and spatial navigation. To reconcile the cross-species differences observed in the presence and properties of theta, we recorded hippocampal local field potentials in rats and ferrets during auditory and visual localisation tasks designed to vary locomotion and sensory attention. Here, we show that theta oscillations occur during locomotion in both ferrets and rats, however during periods of immobility, theta oscillations persist in the ferret, contrasting starkly with the switch to large irregular activity (LIA) in the rat. Theta during immobility in the ferret is identified as analogous to Type 2 theta that has been observed in rodents due to its sensitivity to atropine, and is modulated by behavioural state with the strongest theta observed during reward epochs. These results demonstrate that even under similar behavioural conditions, differences exist between species in the relationship between theta and behavioural state.

The role of temporal coherence and temporal predictability in the build-up of auditory grouping.

The cochlea decomposes sounds into separate frequency channels, from which the auditory brain must reconstruct the auditory scene. To do this the auditory system must make decisions about which frequency information should be grouped together, and which should remain distinct. Two key cues for grouping are temporal coherence, resulting from coherent changes in power across frequency, and temporal predictability, resulting from regular or predictable changes over time. To test how these cues contribute to the construction of a sound scene we present listeners with a range of precursor sounds, which act to prime the auditory system by providing information about each sounds structure, followed by a fixed masker in which participants were required to detect the presence of an embedded tone. By manipulating temporal coherence and/or temporal predictability in the precursor we assess how prior sound exposure influences subsequent auditory grouping. In Experiment 1, we measure the contribution of temporal predictability by presenting temporally regular or jittered precursors, and temporal coherence by using either narrow or broadband sounds, demonstrating that both independently contribute to masking/unmasking. In Experiment 2, we measure the relative impact of temporal coherence and temporal predictability and ask whether the influence of each in the precursor signifies an enhancement or interference of unmasking. We observed that interfering precursors produced the largest changes to thresholds.

Factors Affecting the Use of Speech Testing in Adult Audiology.

OBJECTIVE: The aim of this study was to evaluate hearing health care professionals' (HHPs) speech testing practices in routine adult audiology services and better understand the facilitators and barriers to speech testing provision. DESIGN: A cross-sectional questionnaire study was conducted. STUDY SAMPLE: A sample (N = 306) of HHPs from the public (64%) and private (36%) sectors in the United Kingdom completed the survey. RESULTS: In the United Kingdom, speech testing practice varied significantly between health sectors. Speech testing was carried out during the audiology assessment by 73.4% of private sector HHPs and 20.4% of those from the public sector. During the hearing aid intervention stage, speech testing was carried out by 56.5% and 26.5% of HHPs from the private and public sectors, respectively. Recognized benefits of speech testing included (a) providing patients with relatable assessment information, (b) guiding hearing aid fitting, and (c) supporting a diagnostic test battery. A lack of clinical time was a key barrier to uptake. CONCLUSIONS: Use of speech testing varies in adult audiology. Results from this study found that the percentage of U.K. HHPs making use of speech tests was low compared to that of other countries. HHPs recognized different benefits of speech testing in audiology practice, but the barriers limiting uptake were often driven by factors derived from decision makers rather than clinical rationale. Privately funded HHPs used speech tests more frequently than those working in the public sector where time and resources are under greater pressure and governed by guidance that does not include a recommendation for speech testing. Therefore, the inclusion of speech testing in national clinical guidelines could increase the consistency of use and facilitate the comparison of practice trends across centers. SUPPLEMENTAL MATERIAL: https://doi.org/10.23641/asha.20044457.

Housing and Environmental Enrichment of the Domestic Ferret: A Multi-Sector Survey.

Ferrets (Mustela putorius furo) are kept and used in multiple sectors of society, but little is known about how they are housed and what environmental enrichment (EE) they may benefit from. We aimed to help guide caretakers about what housing and EE can be provided for ferrets. Through an online questionnaire of ferret caretakers, including pet, laboratory, zoological collection, rescue and working animal sectors internationally, we described ferret housing, opportunities for exploration, EE provision and caretaker opinions on ferrets' preferred EE types, and problematic EE. In total, 754 valid responses from 17 countries were analysed, with most (82.4%) coming from pet owners. Most ferrets were housed socially, with housing varying across sectors from single-level cages to free-range housing in a room or outdoor enclosure; pet owners mostly used multi-level cages. The most commonly reported EE included hammocks, tunnels and tactile interaction with caretakers. Respondents reported that ferrets particularly enjoyed digging substrates, tunnels, human interaction and exploration. The most frequently reported problems were that ingestion of unsuitable chew toys and rubber items could cause internal blockages, narrow tunnels could trap ferrets, and certain fabrics that could catch claws. This suggests a need for increased awareness of the risks of these EE types and for more commercially available safety-tested ferret EE. Scent trails were relatively rarely provided but were reported to be enjoyed and harmless, so we recommend that these should be provided more commonly. Our results suggest that there is scope to improve ferret housing and EE provision to benefit ferret welfare across all sectors.

Sound Localization of World and Head-Centered Space in Ferrets.

The location of sounds can be described in multiple coordinate systems that are defined relative to ourselves, or the world around us. Evidence from neural recordings in animals point toward the existence of both head-centered and world-centered representations of sound location in the brain; however, it is unclear whether such neural representations have perceptual correlates in the sound localization abilities of nonhuman listeners. Here, we establish novel behavioral tests to determine the coordinate systems in which ferrets can localize sounds. We found that ferrets could learn to discriminate between sound locations that were fixed in either world-centered or head-centered space, across wide variations in sound location in the alternative coordinate system. Using probe sounds to assess broader generalization of spatial hearing, we demonstrated that in both head and world-centered tasks, animals used continuous maps of auditory space to guide behavior. Single trial responses of individual animals were sufficiently informative that we could then model sound localization using speaker position in specific coordinate systems and accurately predict ferrets' actions in held-out data. Our results demonstrate that ferrets, an animal model in which neurons are known to be tuned to sound location in egocentric and allocentric reference frames, can also localize sounds in multiple head and world-centered spaces.SIGNIFICANCE STATEMENT Humans can describe the location of sounds either relative to themselves, or in the world, independent of their momentary position. These different spaces are also represented in the activity of neurons in animals, but it is not clear whether nonhuman listeners also perceive both head and world-centered sound location. Here, we designed behavioral tasks in which ferrets discriminated between sounds using their position in the world, or relative to the head. Subjects learnt to solve both problems and generalized sound location in each space when presented with infrequent probe sounds. These findings reveal a perceptual correlate of neural sensitivity previously observed in the ferret brain and establish that, like humans, ferrets can access an auditory map of their local environment.

What can we learn from inactivation studies? Lessons from auditory cortex.

Inactivation experiments in auditory cortex (AC) produce widely varying results that complicate interpretations regarding the precise role of AC in auditory perception and ensuing behaviour. The advent of optogenetic methods in neuroscience offers previously unachievable insight into the mechanisms transforming brain activity into behaviour. With a view to aiding the design and interpretation of future studies in and outside AC, here we discuss the methodological challenges faced in manipulating neural activity. While considering AC's role in auditory behaviour through the prism of inactivation experiments, we consider the factors that confound the interpretation of the effects of inactivation on behaviour, including the species, the type of inactivation, the behavioural task employed, and the exact location of the inactivation.

Experienced hearing aid users' perspectives of assessment and communication within audiology: a qualitative study using digital methods.

OBJECTIVE: To explore experienced hearing aid users' perspectives of audiological assessments and the patient-audiologist communication dynamic during clinical interactions. DESIGN: A qualitative study was implemented incorporating both an online focus group and online semi-structured interviews. Sessions were audio-recorded and transcribed verbatim. Iterative-inductive thematic analysis was carried out to identify themes related to assessment and communication within audiology practice. STUDY SAMPLES: Seven experienced hearing aid users took part in an online focus group and 14 participated in online semi-structured interviews (age range: 22 - 86 years; 9 males, 11 females). RESULTS: Themes related to assessment included the unaided and aided testing procedure and relating tests to real world hearing difficulties. Themes related to communication included the importance of deaf aware communication strategies, explanation of test results and patient centred care in audiology. CONCLUSION: To ensure hearing aid services meet the needs of the service users, we should explore user perspectives and proactively adapt service delivery. This approach should be ongoing, in response to advances in hearing aid technology. Within audiology, experienced hearing aid users' value (1) comprehensive, relatable hearing assessment, (2) deaf aware patient-audiologist communication, (3) accessible services and (4) a personalised approach to recommend suitable technology and address patient specific aspects of hearing loss.

Audiovisual integration in macaque face patch neurons.

Primate social communication depends on the perceptual integration of visual and auditory cues, reflected in the multimodal mixing of sensory signals in certain cortical areas. The macaque cortical face patch network, identified through visual, face-selective responses measured with fMRI, is assumed to contribute to visual social interactions. However, whether face patch neurons are also influenced by acoustic information, such as the auditory component of a natural vocalization, remains unknown. Here, we recorded single-unit activity in the anterior fundus (AF) face patch, in the superior temporal sulcus, and anterior medial (AM) face patch, on the undersurface of the temporal lobe, in macaques presented with audiovisual, visual-only, and auditory-only renditions of natural movies of macaques vocalizing. The results revealed that 76% of neurons in face patch AF were significantly influenced by the auditory component of the movie, most often through enhancement of visual responses but sometimes in response to the auditory stimulus alone. By contrast, few neurons in face patch AM exhibited significant auditory responses or modulation. Control experiments in AF used an animated macaque avatar to demonstrate, first, that the structural elements of the face were often essential for audiovisual modulation and, second, that the temporal modulation of the acoustic stimulus was more important than its frequency spectrum. Together, these results identify a striking contrast between two face patches and specifically identify AF as playing a potential role in the integration of audiovisual cues during natural modes of social communication.

Training enhances the ability of listeners to exploit visual information for auditory scene analysis.

The ability to use temporal relationships between cross-modal cues facilitates perception and behavior. Previously we observed that temporally correlated changes in the size of a visual stimulus and the intensity in an auditory stimulus influenced the ability of listeners to perform an auditory selective attention task (Maddox, Atilgan, Bizley, & Lee, 2015). Participants detected timbral changes in a target sound while ignoring those in a simultaneously presented masker. When the visual stimulus was temporally coherent with the target sound, performance was significantly better than when the visual stimulus was temporally coherent with the masker, despite the visual stimulus conveying no task-relevant information. Here, we trained observers to detect audiovisual temporal coherence and asked whether this changed the way in which they were able to exploit visual information in the auditory selective attention task. We observed that after training, participants were able to benefit from temporal coherence between the visual stimulus and both the target and masker streams, relative to the condition in which the visual stimulus was coherent with neither sound. However, we did not observe such changes in a second group that were trained to discriminate modulation rate differences between temporally coherent audiovisual streams, although they did show an improvement in their overall performance. A control group did not change their performance between pretest and post-test and did not change how they exploited visual information. These results provide insights into how crossmodal experience may optimize multisensory integration.

Seasonal weight changes in laboratory ferrets.

Ferrets (Mustela putorius furo) are a valuable animal model used in biomedical research. Like many animals, ferrets undergo significant variation in body weight seasonally, affected by photoperiod, and these variations complicate the use weight as an indicator of health status. To overcome this requires a better understanding of these seasonal weight changes. We provide a normative weight data set for the female ferret accounting for seasonal changes, and also investigate the effect of fluid regulation on weight change. Female ferrets (n = 39) underwent behavioural testing from May 2017 to August 2019 and were weighed daily, while housed in an animal care facility with controlled light exposure. In the winter (October to March), animals experienced 10 hours of light and 14 hours of dark, while in summer (March to October), this contingency was reversed. Individual animals varied in their body weight from approximately 700 to 1200 g. However, weights fluctuated with light cycle, with animals losing weight in summer, and gaining weight in winter such that they fluctuated between approximately 80% and 120% of their long-term average. Ferrets were weighed as part of their health assessment while experiencing water regulation for behavioural training. Water regulation superimposed additional weight changes on these seasonal fluctuations, with weight loss during the 5-day water regulation period being greater in summer than winter. Analysing the data with a Generalised Linear Model confirmed that the percentage decrease in weight per week was relatively constant throughout the summer months, while the percentage increase in body weight per week in winter decreased through the season. Finally, we noted that the timing of oestrus was reliably triggered by the increase in day length in spring. These data establish a normative benchmark for seasonal weight variation in female ferrets that can be incorporated into the health assessment of an animal's condition.

Auditory Neuroscience: Unravelling How the Brain Gives Sound Meaning.

The brain must be able to assign sounds in the world to behaviourally meaningful categories. A new study has revealed that sensory pathways represent category information, but that selectivity for sound classes emerges first in the frontal cortex.

Dorsal prefrontal and premotor cortex of the ferret as defined by distinctive patterns of thalamo-cortical projections.

Recent studies of the neurobiology of the dorsal frontal cortex (FC) of the ferret have illuminated its key role in the attention network, top-down cognitive control of sensory processing, and goal directed behavior. To elucidate the neuroanatomical regions of the dorsal FC, and delineate the boundary between premotor cortex (PMC) and dorsal prefrontal cortex (dPFC), we placed retrograde tracers in adult ferret dorsal FC anterior to primary motor cortex and analyzed thalamo-cortical connectivity. Cyto- and myeloarchitectural differences across dorsal FC and the distinctive projection patterns from thalamic nuclei, especially from the subnuclei of the medial dorsal (MD) nucleus and the ventral thalamic nuclear group, make it possible to clearly differentiate three separate dorsal FC fields anterior to primary motor cortex: polar dPFC (dPFCpol), dPFC, and PMC. Based on the thalamic connectivity, there is a striking similarity of the ferret's dorsal FC fields with other species. This possible homology opens up new questions for future comparative neuroanatomical and functional studies.

Does 'playtime' reduce stimulus-seeking and other boredom-like behaviour in laboratory ferrets?

Much environmental enrichment for laboratory animals is intended to enhance animal welfare and normalcy by providing stimulation to reduce 'boredom'. Behavioural manifestations of boredom include restless sensation-seeking behaviours combined with indicators of sub-optimal arousal. Here we explored whether these signs could be reduced by extra daily play opportunity in laboratory ferrets. Specifically, we hypothesised that playtime would reduce restlessness, aggression, sensation-seeking and awake drowsiness, even 24h later in the homecage. Female ferrets (n = 14) were group housed in enriched multi-level cages. Playtime involved exploring a room containing a ball pool, paper bags, balls containing bells, and a familiar interactive human for 1h. This was repeated on three consecutive mornings, and on the fourth morning, homecage behaviour was compared between ferrets who had experienced the playtime treatment versus control cagemates who had not. Their investigation of stimuli (positive = mouse odour or ball; ambiguous = empty bottle or tea-strainer; and negative = peppermint or bitter apple odour) was also recorded. We then swapped treatments, creating a paired experimental design. Ferrets under control conditions lay awake with their eyes open and screeched significantly more, but slept and sat/stood less, than following playtime. They also contacted negative and ambiguous stimuli significantly more under control conditions than they did following playtime; contact with positive stimuli showed no effects. Attempts to blind the observer to treatments were unsuccessful, so replication is required, but the findings suggest that playtime may have reduced both sub-optimal arousal and restless sensation seeking behaviour, consistent with reducing boredom.

Neurons in primary auditory cortex represent sound source location in a cue-invariant manner.

Auditory cortex is required for sound localisation, but how neural firing in auditory cortex underlies our perception of sound sources in space remains unclear. Specifically, whether neurons in auditory cortex represent spatial cues or an integrated representation of auditory space across cues is not known. Here, we measured the spatial receptive fields of neurons in primary auditory cortex (A1) while ferrets performed a relative localisation task. Manipulating the availability of binaural and spectral localisation cues had little impact on ferrets' performance, or on neural spatial tuning. A subpopulation of neurons encoded spatial position consistently across localisation cue type. Furthermore, neural firing pattern decoders outperformed two-channel model decoders using population activity. Together, these observations suggest that A1 encodes the location of sound sources, as opposed to spatial cue values.

Sound identity is represented robustly in auditory cortex during perceptual constancy.

Perceptual constancy requires neural representations that are selective for object identity, but also tolerant across identity-preserving transformations. How such representations arise in the brain and support perception remains unclear. Here, we study tolerant representation of sound identity in the auditory system by recording neural activity in auditory cortex of ferrets during perceptual constancy. Ferrets generalize vowel identity across variations in fundamental frequency, sound level and location, while neurons represent sound identity robustly across acoustic variations. Stimulus features are encoded with distinct time-courses in all conditions, however encoding of sound identity is delayed when animals fail to generalize and during passive listening. Neurons also encode information about task-irrelevant sound features, as well as animals' choices and accuracy, while population decoding out-performs animals' behavior. Our results show that during perceptual constancy, sound identity is represented robustly in auditory cortex across widely varying conditions, and behavioral generalization requires conserved timing of identity information.