Biology subjects

Billig, A. J.

Publications and source records attributed to Billig, A. J..

11 recordsLinked to original sources

bioRxiv2026

Neural Bases for Working Memory of Natural Sound Textures

Holding sound objects in mind is critical to understanding the sound world around us. Auditory texture perception is thought to rely on extracting statistical properties of sounds over time, raising the question of how encoding duration influences subsequent maintenance of auditory texture information. We investigated this question using behavioural performance and fMRI while participants performed two delayed match-to-sample tasks: a texture discrimination and a comparison loudness discrimination task. In the texture task, participants judged whether two sequentially presented sounds belonged to the same texture type, whereas in the loudness task, participants judged whether the sounds, drawn from the same texture type, had the same loudness. Stimuli were presented for either 0.1s or 2s. Discrimination sensitivity increased with duration in both tasks, but more strongly for texture discrimination. fMRI analysis revealed distinct effects of duration on univariate and multivariate activity in the auditory cortex and medial temporal lobe (MTL) during maintenance. We found no univariate duration effect in the auditory cortex during maintenance, but multivariate patterns encoded texture category more strongly for longer stimuli, regardless of task. In contrast, MTL activity was modulated by sound duration in both tasks, but there was no effect of duration on texture category decoding. There was a task effect in MTL where multivariate patterns in posterior hippocampal and parahippocampal regions distinguished texture from loudness tasks following 2s stimuli. Together, these findings show effects of duration on sound texture representations during maintenance and that MTL representations reflect the behavioural context in which that information is maintained.

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bioRxiv2025

Brain-wide single-neuron bases of working memory for sounds in humans

In order to understand the constantly changing acoustic world our brains must maintain elements of auditory scenes in memory. The neural mechanisms for this fundamental process remain unclear. Here, we report human intracranial recordings of 1269 single neurons while participants performed a non-verbal auditory working memory task that required adjustment of a tone frequency to match a target. We found neurons within hippocampus, insula and cingulate cortex, for which firing rates were modulated at different phases of the task, particularly during maintenance and adjustment. For the majority of the neurons modulated during maintenance there was a striking suppression of activity rather than increased activity. Across the entire neuronal population, state-space analysis demonstrated attractor-like states corresponding to different task phases. Behaviorally, more neurons were modulated at the beginning of the maintenance phase in trials when participants performed better. State-space analysis was consistent with greater attractor-like activity during the adjustment phase supporting better performance. These data support the existence of a widely distributed neural code for auditory working memory that determines related behavior based on attractor-like states.

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bioRxiv2025

Brain Representations of Natural Sound Statistics

Natural sound textures (e.g., rain, crackling fire) are perceptually defined by time-averaged summary statistics. While previous studies have examined neural responses to natural sounds, little is known regarding the neural processing of the statistics underlying these sounds. To study neuronal correlates of these statistics, we measured brain responses to synthetic sound textures in which statistical structure was systematically varied while preserving the texture category. Using two fMRI experiments (males and females), we examined neural responses along the ascending auditory pathway, within auditory cortex and medial temporal lobe (MTL) regions implicated in pattern analysis. In Experiment 1, we parametrically varied the full set of texture statistics, creating sounds with different levels of naturalness. In Experiment 2, we selectively manipulated high-level statistics (cochlear skewness and kurtosis, cochlear and modulation correlations) while holding low-level statistics (cochlear mean and modulation power) constant. Increasing texture naturalness produced graded increases in BOLD responses across bilateral primary and nonprimary auditory cortex in both experiments, although overall responses were weaker in Experiment 2. This reduction suggests that low-level statistics contribute substantially to response magnitude, even though higher-order statistics are sufficient to elicit graded responses. We also observed modulation in MTL regions, including entorhinal cortex, in Experiment 1. Moreover, functional connectivity between hippocampus and auditory cortex increased for more degraded (less natural) textures, suggesting a modulatory rather than representational role for MTL in texture processing. Together, these findings show that sensitivity to texture statistics is distributed across the auditory cortex and highlight MTL-auditory interactions when texture structure is ambiguous. Significant StatementNatural sound textures such as rain or crackling fire are perceptually defined by time-averaged summary statistics that support efficient auditory perception, yet how the human brain represents these statistics remains unclear. Using fMRI and synthetic sound textures in which statistical structure was systematically manipulated, we found that both primary and nonprimary auditory cortex were sensitive to texture statistics, exhibiting a graded and distributed representation of these acoustic features. We also observed increased functional connectivity between the hippocampus and auditory regions when texture structure was degraded or the sounds were unnatural. Together, these results indicate that sound texture statistics are encoded across multiple levels of auditory cortex and further suggest a modulatory role for hippocampus under conditions of heightened perceptual uncertainty.

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bioRxiv2025

Brain bases for navigating acoustic features

Whether physical navigation shares neural substrates with mental travel in other behaviourally relevant domains is debated. With respect to sound, pure-tone working memory in humans elicits hippocampal as well as auditory cortical and inferior frontal activity, and rodent work suggests that hippocampal cells that usually track an animals physical location can also map to tone frequency when task-relevant. We generated a sound dimension based on the density of random-frequency tones in a stack, resulting in a percept ranging from low- ("beepy") to high-density ("noisy"). We established that unlike tone frequency, which listeners automatically associate with vertical position, this density dimension elicited no consistent spatial mapping. During functional magnetic resonance imaging, human participants held in mind the density of a series of tone stacks and, after a short maintenance period, adjusted further stacks to match the target ("navigation"). Density of the currently heard sound was represented most strongly in bilateral non-primary auditory cortex, specifically bilateral planum polare, while density of the maintained target was represented in right anterior hippocampus and left inferior temporal gyrus. Encoding and maintenance activity in bilateral hippocampus, inferior frontal gyrus, planum polare and posterior cingulate was positively associated with subsequent navigation success. Bilateral inferior frontal gyrus and hippocampus were among regions with elevated activity during adjustment, compared to a parity-judgment condition with closely matched acoustics and motor demands. Bilateral orbitofrontal cortex was more active when navigation was toward a target density than when participants adjusted density in a control condition with no particular target. We find that self-initiated travel along a non-spatial auditory dimension engages a brain system overlapping with that supporting physical navigation. Key PointsO_LIWork in rodents suggests that navigation in physical space and the active analysis of sounds share a neural substrate in the hippocampus, supporting the use of common computational mechanisms. C_LIO_LIWe examined the human brain system for navigation through an acoustic environment to a remembered target. C_LIO_LIIn addition to high-level auditory cortex we demonstrate involvement of the hippocampus in acoustic navigation along with other sites in frontal and cingulate cortex that also support physical navigation. C_LI

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bioRxiv2021

A specific relationship between musical sophistication and auditory working memory

Musical engagement may be associated with better listening skills, such as the perception of and working memory for notes, in addition to the appreciation of musical rules. The nature and extent of this association is controversial. In this study we assessed the relationship between musical engagement and both sound perception and working memory. We developed a task to measure auditory perception and working memory for sound using a behavioural measure for both, precision. We measured the correlation between these tasks and musical sophistication based on a validated measure (the Goldsmiths Musical Sophistication Index) that can be applied to populations of both musicians and non-musicians. The data show that musical sophistication accounts for 21% of the variance in the precision of working memory for frequency in an analysis that accounts for age and non-verbal intelligence. Musical sophistication was not significantly associated with the precision of working memory for amplitude modulation rate or with the precision of perception of either acoustic feature. The work supports a specific association between musical sophistication and working memory for sound frequency.

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bioRxiv2020

An online headphone screening test based on dichotic pitch

Online experimental platforms can be used as an alternative, or complement, to lab-based research. However, when conducting auditory experiments via online methods, the researcher has limited control over the participants listening environment. We offer a new method to probe one aspect of that environment, headphone use. Headphones not only provide better control of sound presentation but can also "shield" the listener from background noise. Here we present a rapid (< 3 minute) headphone screening test based on Huggins Pitch (HP), a perceptual phenomenon that can only be detected when stimuli are presented dichotically. We validate this test using a cohort of "Trusted" online participants who completed the test using both headphones and loudspeakers. The same participants were also used to test an existing headphone test (AP test; Woods et al., 2017, Attention Perception Psychophysics). We demonstrate that compared to the AP test, the HP test has a higher selectivity for headphone users, rendering it as a compelling alternative to existing methods. Overall, the new HP test correctly detects 80% of headphone users and has a false positive rate of 20%. Moreover, we demonstrate that combining the HP test with an additional test - either the AP test or an alternative based on a beat test (BT) - can lower the false positive rate to [~]7%. This should be useful in situations where headphone use is particularly critical (e.g. dichotic or spatial manipulations). Code for implementing the new tests is publicly available in JavaScript and through Gorilla (gorilla.sc).

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bioRxiv2020

Oscillatory correlates of auditory working memory examined with human electrocorticography

This work examines how sounds are held in auditory working memory (AWM) in humans by examining oscillatory local field potentials (LFPs) in candidate brain regions. Previous fMRI studies by our group demonstrated blood oxygenation level-dependent (BOLD) response increases during maintenance in auditory cortex, inferior frontal cortex and the hippocampus using a paradigm with a delay period greater than 10s. The relationship between such BOLD changes and ensemble activity in different frequency bands is complex, and the long delay period raised the possibility that long-term memory mechanisms were engaged. Here we assessed LFPs in different frequency bands in six subjects with recordings from all candidate brain regions using a paradigm with a short delay period of 3 s. Sustained delay activity was demonstrated in all areas, with different patterns in the different areas. Enhancement in low frequency (delta) power and suppression across higher frequencies (beta/gamma) were demonstrated in primary auditory cortex in medial Heschls gyrus (HG) whilst non-primary cortex showed patterns of enhancement and suppression that altered at different levels of the auditory hierarchy from lateral HG to superior- and middle-temporal gyrus. Inferior frontal cortex showed increasing suppression with increasing frequency. The hippocampus and parahippocampal gyrus showed low frequency increases and high frequency decreases in oscillatory activity. The work demonstrates sustained activity patterns that can only be explained by AWM maintenance, with prominent low-frequency increases in medial temporal lobe regions.

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bioRxiv2020

Common Fronto-temporal Effective Connectivity in Humans and Monkeys

Cognitive pathways supporting human language and declarative memory are thought to have uniquely evolutionarily differentiated in our species. However, cross-species comparisons are missing on site-specific effective connectivity between regions important for cognition. We harnessed a new approach using functional imaging to visualize the impact of direct electrical brain stimulation in human neurosurgery patients. Applying the same approach with macaque monkeys, we found remarkably comparable patterns of effective connectivity between auditory cortex and ventro-lateral prefrontal cortex (vlPFC) and parahippocampal cortex in both species. Moreover, in humans electrical tractography revealed rapid evoked potentials in vlPFC from stimulating auditory cortex and speech sounds drove vlPFC, consistent with prior evidence in monkeys of direct projections from auditory cortex to vocalization responsive regions in vlPFC. The results identify a common effective connectivity signature that from auditory cortex is equally direct to vlPFC and indirect to the hippocampus (via parahippocampal cortex) in human and nonhuman primates. HighlightsO_LIPrivileged human auditory to inferior frontal connectivity, linked to monkeys C_LIO_LICommon auditory to parahippocampal effective connectivity in both species C_LIO_LIGreater lateralization in human effective connectivity, more symmetrical in monkeys C_LIO_LIHuman fronto-temporal network function rooted in evolutionarily conserved signature C_LI eTOC short summaryFunctional connectivity between regions crucial for language and declarative memory is thought to have substantially differentiated in humans. Using a new technique to similarly visualize directional effective connectivity in humans and monkeys, we found remarkably comparable connectivity patterns in both species between fronto-temporal regions crucial for cognition.

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bioRxiv2019

A sound-sensitive source of alpha oscillations in human non-primary auditory cortex

The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschls gyrus (HG) with pronounced induced high-frequency (70-150 Hz) activity and short-latency responses that phase-lock to rapid transient sounds. Low-frequency neural oscillations are also relevant to stimulus processing and information flow, however their distribution within auditory cortex has not been established. Alpha activity (7-14 Hz) in particular has been associated with processes that may differentially engage earlier versus later levels of the cortical hierarchy, including functional inhibition and the communication of sensory predictions. These theories derive largely from the study of occipitoparietal sources readily detectable in scalp electroencephalography. To characterize the anatomical basis and functional significance of less accessible temporal-lobe alpha activity we analyzed responses to sentences in seven human adults (four female) with epilepsy who had been implanted with electrodes in superior temporal cortex. In contrast to primary cortex in posteromedial HG, a non-primary field in anterolateral HG was characterized by high spontaneous alpha activity that was strongly suppressed during auditory stimulation. Alpha-power suppression decreased with distance from anterolateral HG throughout superior temporal cortex, and was more pronounced for clear compared to degraded speech. This suppression could not be accounted for solely by a change in the slope of the power spectrum. The differential manifestation and stimulus-sensitivity of alpha oscillations across auditory fields should be accounted for in theories of their generation and function.\n\nSignificance StatementTo understand how auditory cortex is organized in support of perception, we recorded from patients implanted with electrodes for clinical reasons. This allowed measurement of activity in brain regions at different levels of sensory processing. Oscillations in the alpha range (7-14 Hz) have been associated with functions including sensory prediction and inhibition of regions handling irrelevant information, but their distribution within auditory cortex is not known. A key finding was that these oscillations dominated in one particular non-primary field, anterolateral Heschls gyrus, and were suppressed when subjects listened to sentences. These results build on our knowledge of the functional organization of auditory cortex and provide anatomical constraints on theories of the generation and function of alpha oscillations.

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bioRxiv2018

Effect of chronic stimulation and stimulus level on temporal processing by cochlear implant listeners

A series of experiments investigated potential changes in temporal processing during the months following activation of a cochlear implant (CI) and as a function of stimulus level. Experiment 1 tested patients on the day of implant activation and two and six months later. All stimuli were presented using direct stimulation of a single apical electrode. The dependent variables were rate discrimination ratios (RDRs) for pulse trains with rates centred on 120 pulses per second (pps), obtained using an adaptive procedure, and a measure of the upper limit of temporal pitch, obtained using a pitch-ranking procedure.\n\nAll stimuli were presented at their most comfortable level (MCL). RDRs decreased from 1.23 to 1.16 and the upper limit increased from 357 to 485 pps from 0 to 2 months post-activation, with no overall change from 2 to 6 months. Because MCLs and hence the testing level increased across sessions, two further experiments investigated whether the performance changes observed across sessions could be due to level differences. Experiment 2 re-tested a subset of subjects at 9 months post-activation, using current levels similar to those used at 0 months. Although the stimuli sounded softer, some subjects showed lower RDRs and/or higher upper limits at this re-test. Experiment 3 measured RDRs and the upper limit for a separate group of subjects at levels equal to 60%, 80%, and 100% of the dynamic range. RDRs decreased with increasing level. The upper limit increased with increasing level for most subjects, with two notable exceptions. Implications of the results for temporal plasticity are discussed, along with possible influences of the effects of level and of across-session learning.

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bioRxiv2017

Neural decoding of bistable sounds reveals an effect of intention on perceptual organization

Auditory signals arrive at the ear as a mixture that the brain must decompose into distinct sources, based to a large extent on acoustic properties of the sounds. An important question concerns whether listeners have voluntary control over how many sources they perceive. This has been studied using pure tones H and L presented in the repeating pattern HLH-HLH-, which can form a bistable percept, heard either as an integrated whole (HLH-) or as segregated into high (H-H-) and low (-L--) sequences. Although instructing listeners to try to integrate or segregate sounds affects reports of what they hear, this could reflect a response bias rather than a perceptual effect. We had human listeners (15 males, 12 females) continuously report their perception of such sequences and recorded neural activity using magneto-encephalography. During neutral listening, a classifier trained on patterns of neural activity distinguished between periods of integrated and segregated perception. In other conditions, participants tried to influence their perception by allocating attention either to the whole sequence, or to a subset of the sounds. They reported hearing the desired percept for a greater proportion of time than when listening neutrally. Critically, neural activity supported these reports; stimulus-locked brain responses in auditory cortex were more likely to resemble the signature of segregation when participants tried to hear segregation than when attempting to perceive integration. These results indicate that listeners can influence how many sound sources they perceive, as reflected in neural responses that track both the input and its perceptual organization.\n\nSignificance StatementCan we consciously influence our perception of the external world? We address this question using sound sequences that can be heard either as coming from a single source, or as two distinct auditory streams. Listeners reported spontaneous changes in their perception between these two interpretations while we recorded neural activity to identify signatures of such integration and segregation. They also indicated that they could, to some extent, choose between these alternatives. This claim was supported by corresponding changes in responses in auditory cortex. By linking neural and behavioral correlates of perception we demonstrate that the number of objects we perceive can depend not only on the physical attributes of our environment, but also on how we intend to experience it.

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