Biology subjects

Shamma, S.

Publications and source records attributed to Shamma, S..

16 recordsLinked to original sources

bioRxiv2026

AUDITORY-MOTOR SURPRISAL REVEALS LEARNING ACROSS MULTIPLE TIMESCALES DURING EXPLORATION AND PRODUCTION

Auditory-motor learning is critical for mastering the production of complex sounds, such as speaking and playing music. It is anchored upon internal models of interactions between actions and their sensory consequences, which are fine-tuned by minimizing the errors between the predicted and received sound. Here, we investigated the neural dynamics of sensorimotor learning by manipulating sensorimotor surprisal, with high surprisal defined as unexpected changes in the mapping between actions and their auditory outcomes. Participants performed a piano-playing task in which the key-to-pitch mapping switched unpredictably among three configurations, creating a dynamic sensorimotor environment that required ongoing adaptation. At the change boundaries, a signature of violated motor-to-auditory predictions was found in the auditory evoked responses at N100, which could not be attributed to either purely auditory surprisals or motor execution errors. This prediction error is modulated by short-term context, with greater error responses following longer periods of no map change, indicating that the brain continuously tracks short-term map contexts and rapidly adapts to them. In contrast, 30 minutes of extended goal-directed training on a single key-pitch map modulated P50 amplitude only for the trained map, a modulation that can be explained by a slow, training-driven update of the sensorimotor map. Hence, while auditory predictions from motor actions can be implicitly learned within short-term contexts for rapid adaptation, the complementary process of building a reliable sensorimotor map requires targeted training sustained over time. Our approach of studying auditory-motor surprisal in time-varying sequences reveals that auditory-motor learning is fast, context-sensitive, and shaped by both short- and long-term experience. Significance statementUnderstanding how the brain links motor actions with their sensory consequences is key to explaining how complex skills are acquired and subsequently adapted to changing environments. Yet, the neural mechanisms underpinning the evolution of internal sensorimotor associations across different timescales remain to be elucidated. Here, we extend the concept of surprisal, traditionally used in studies of perception, to the sensorimotor domain, where it is elicited by violations of expectations about the sensory outcome of an action. These expectations are generated by an internal model of sensorimotor associations that must nevertheless remain sufficiently flexible to enable rapid adaptation. Results show that surprisal responses are modulated differently by short-term sensory feedback and longer-term training, via two distinct neural mechanisms underlying adaptation and long-term sensorimotor map updates. These findings advance our understanding of the neural dynamics of sensorimotor learning and inform the design of emerging sensorimotor technologies, enabling novel forms of human-machine interaction and creative applications.

neuroscience↗

bioRxiv2026

Neural Decoding of Musical Engagement Reveals Tension-Release Dynamics

Music listening is one of the most compelling and rewarding activities humans engage in spontaneously. But what exactly catches people"s attention when listening to music remains unclear. Musicologists have argued that tension-release dynamics in music constitute crucial features of the listening experience. They arise from the intertwining of different low-level and high-level features and sit at the core of music enjoyment by engaging listeners dynamically. This study aims to characterize the relationship between tension dynamics and engagement during naturalistic music listening. Using canonical correlation analysis, we decoded the music envelope from EEG and ECoG responses and found that musical tension patterns, as reported by listeners, were predictive of fluctuations in the coupling between the music and the neural response. Importantly, tension dynamics were significantly correlated with neural measures of envelope tracking even after controlling for loudness and musical expectations, confirming the specific and crucial role of musical tension in engaging listeners. These results shed new light on how musical structure gives rise to internal response modulations that, in turn, dynamically reflect musical engagement. This interplay may underlie the pervasive and emotionally rewarding nature of music. Significance StatementThis work addresses a fundamental question in cognition: how engagement dynamically modulates complex auditory input processing. We investigate this issue within the well-controlled yet ecologically valid context of music perception. At the core of the musical experience lies the perception of tension - the shifting sense of expectancy, instability, and resolution that guides listening across time. We show that fluctuations in musical tension, shaped by musical structure, reliably predict modulations of auditory engagement, thereby illuminating an understudied phenomenon: what makes music engaging.

neuroscience↗

bioRxiv2025

Similar Dynamic Frontal Cortex Representations of Auditory Stimuli Cueing Opposite Actions and Rewards

Frontal Cortex (FC) plays a pivotal role in controlling actions and their dynamics in response to incoming sensory stimuli. We explored FC representations of the same stimuli when signifying diametrically opposite behavioral meanings depending on task context. Two groups of ferrets performed Go-NoGo auditory categorization tasks with opposite contingencies and rewards, and varied stimuli. Remarkably, despite the opposite stimulus-action associations, single-unit responses were similar across all tasks, being more sustained and stronger to (Target) sounds signaling a change in action, than to (Reference) sounds indicating maintenance of ongoing actions, especially during task engagement. Three major dynamic response profiles were extracted from the overall responses, and their combination defined separate neuronal clusters that exhibited different roles in relation to task events. Decoding based on the temporal structure of the population responses revealed distinct decoders that were aligned to different task events. Furthermore, the {beta}-band power, extracted from the FC local field potentials, was similarly and strongly modulated during Target stimuli in all tasks despite opposite behavioral actions. Based on these findings, we propose a model of pathway-specific functional projections from the tripartite FC neuronal clusters to the basal ganglia that is consistent with previous evidence for the conjoint roles of the FC and striatum in adaptive motor control.

neuroscience↗

bioRxiv2024

Premotor cortex hemodynamics reflect internal auditory category, not reported category

1In sensory decision-making tasks, animals decisions are driven by perception, but also by non-perceptual factors. Because of external and internal noise, stimuli may be internally misclassified, leading to perceptual errors. But other, non-sensory factors such as impulsivity or exploratory behavior can lead to non-perceptual errors. Here we exploited the neural traces of these errors in frontal cortex to provide insights into their role in sensory decision making. Using functional ultrasound imaging (fUS), we investigated how the premotor cortex (PMC) in ferrets represents stimuli in a categorization task, varying the difficulty in order to manipulate the rates of perceptual errors. We found that PMC activity reflects the objective (and not the chosen) stimulus category on incorrect Easy trials, when non-perceptual errors are more likely. In contrast, PMC responses correlate with the chosen category (and not objective category) on incorrect Difficult trials, when perceptual errors are more likely. These results suggest that PMC encodes the ferrets perceptual decision but not necessarily the final motor decision. Perceptual errors could be refined further by assessing licking patterns, but licking patterns alone did not explain the effect. This study advances our understanding of the functional role of the frontal cortex in decision making, suggesting that the PMC integrates sensory inputs to guide behavior based on perceptual, rather than motivational, information.

neuroscience↗

bioRxiv2024

Temporal-Coherence Induces Binding in Responses to Sound Sequences in Ferret Auditory Cortex

Binding the attributes of a sensory source is necessary to perceive it as a unified entity, one that can be attended to and extracted from its surrounding scene. In auditory perception, this is the essence of the cocktail party problem in which a listener segregates one speaker from a mixture of voices, or a musical stream from simultaneous others. It is postulated that coherence of the temporal modulations of a sources features is necessary to bind them. The focus of this study is on the role of temporal-coherence in binding and segregation, and specifically as evidenced by the neural correlates of rapid plasticity that enhance cortical responses among synchronized neurons, while suppressing them among asynchronized ones. In a first experiment, we find that attention to a sound sequence rapidly binds it to other coherent sequences while suppressing nearby incoherent sequences, thus enhancing the contrast between the two groups. In a second experiment, a sequence of synchronized multi-tone complexes, embedded in a cloud of randomly dispersed background of desynchronized tones, perceptually and neurally pops-out after a fraction of a second highlighting the binding among its coherent tones against the incoherent background. These findings demonstrate the role of temporal-coherence in binding and segregation.

neuroscience↗

bioRxiv2024

Temporal Coherence Shapes Cortical Responses to Speech Mixtures in a Ferret Cocktail Party

Segregation of complex sounds such as speech, music and animal vocalizations as they simultaneously emanate from multiple sources (referred to as the "cocktail party problem") is a remarkable ability that is common in humans and animals alike. The neural underpinnings of this process have been extensively studied behaviorally and physiologically in non-human animals primarily with simplified sounds (tones and noise sequences). In humans, segregation experiments utilizing more complex speech mixtures are common; but physiological experiments have relied on EEG/MEG/ECoG recordings that sample activity from thousands of neurons, often obscuring the detailed processes that give rise to the observed segregation. The present study combines the insights from animal single-unit physiology with segregation of speech-like mixtures. Ferrets were trained to attend to a female voice and detect a target word, both in presence or absence of a concurrent, equally salient male voice. Single neuron recordings were obtained from primary and secondary ferret auditory cortical fields, as well as frontal cortex. During task performance, representation of the female words became more enhanced relative to those of the (distractor) male in all cortical regions, especially in the higher auditory cortical field. Analysis of the temporal and spectral response characteristics during task performance reveals how speech segregation gradually emerges in the auditory cortex. A computational model evaluated on the same voice mixtures replicates and extends these results to different attentional targets (attention to female or male voices). These findings are consistent with the temporal coherence theory whereby attention to a target voice anchors neural activity in cortical networks hence binding together channels that are coherently temporally-modulated with the target, and ultimately forming a common auditory stream.

neuroscience↗

bioRxiv2023

Decoding contextual influences on auditory perception from primary auditory cortex

Perception can be highly dependent on stimulus context, but whether and how sensory areas encode the context remains uncertain. We used an ambiguous auditory stimulus - a tritone pair - to investigate the neural activity associated with a preceding contextual stimulus that strongly influenced the tritone pairs perception: either as an ascending or a descending step in pitch. We recorded single-unit responses from a population of auditory cortical cells in awake ferrets listening to the tritone pairs preceded by the contextual stimulus. We find that the responses adapt locally to the contextual stimulus, consistent with human MEG recordings from the auditory cortex under the same conditions. Decoding the population responses demonstrates that cells responding to pitch-class-changes are able to predict well the context-sensitive percept of the tritone pairs. Conversely, decoding the individual pitch-class representations and taking their distance in the circular Shepard tone space predicts the opposite of the percept. The various percepts can be readily captured and explained by a neural model of cortical activity based on populations of adapting, pitch-class and pitch-class-direction cells, aligned with the neurophysiological responses. Together, these decoding and model results suggest that contextual influences on perception may well be already encoded at the level of the primary sensory cortices, reflecting basic neural response properties commonly found in these areas.

neuroscience↗

bioRxiv2022

Dynamics and maintenance of categorical responses in primary auditory cortex during task engagement

Grouping sets of sounds into relevant categories is an important cognitive ability that facilitates the association of stimuli with appropriate goal-directed behavioral responses. In perceptual tasks, a prominent role of primary auditory cortex (A1) is to multiplex the encoding of sound sensory features and task variables. Here we investigated the involvement of A1 in initiating sound categorization. We trained ferrets to discriminate click trains of different rates in a Go/No-Go delayed categorization task and recorded neural activity during both active behavior and passive exposure to the same sounds. Purely categorical response components were extracted and analyzed separately from sensory responses to reveal their contributions to the overall population response throughout the trials. We found that population-level representation of Go/No-Go behavioral categories emerged during sound presentation and was present in both active behavioral and passive states. However, upon task engagement, categorical responses to the No-Go category became suppressed, leading to an asymmetrical representation of the Go stimuli relative to the No-Go sounds and prestimulus baseline. At stimulus offset, the population code changed abruptly but categorical representation was maintained during the delay period. Categorical responses extracted from the stimulus period correlated with the ones found in the delay epoch, suggesting an early contribution of A1 to stimulus categorization.

neuroscience↗

bioRxiv2022

Neural basis of melodic learning explains cross-cultural regularities in musical scales

SummarySeeking exposure to unfamiliar experiences constitutes an essential aspect of the human condition, and the brain must adapt to the constantly changing environment by learning the evolving statistical patterns emerging from it. Cultures are shaped by norms and conventions and therefore novel exposure to an unfamiliar culture induces a type of learning that is often described as implicit: when exposed to a set of stimuli constrained by unspoken rules, cognitive systems must rapidly build a mental representation of the underlying grammar. Music offers a unique opportunity to investigate this implicit statistical learning, as sequences of tones forming melodies exhibit structural properties learned by listeners during short- and long-term exposure. Understanding which specific structural properties of music enhance learning in naturalistic learning conditions reveals hard-wired properties of cognitive systems while elucidating the prevalence of these features across cultural variations. Here we provide behavioral and neural evidence that the prevalence of non-uniform musical scales may be explained by their facilitating effects on melodic learning. In this study, melodies were generated using an artificial grammar with either a uniform (rare) or non-uniform (prevalent) scale. After a short exposure phase, listeners had to detect ungrammatical new melodies while their EEG responses were recorded. Listeners performance on the task suggested that the extent of statistical learning during music listening depended on the musical scale context: non-uniform scales yielded better syntactic learning. This behavioral effect was mirrored by enhanced encoding of musical syntax in the context of non-uniform scales, which further suggests that their prevalence stems from fundamental properties of learning.

neuroscience↗

bioRxiv2021

Binding the acoustic features of an auditory source through temporal coherence

Numerous studies have suggested that the perception of a target sound source can only be segregated from a complex acoustic background if the acoustic features underlying its perceptual attributes (e.g., pitch, location, and timbre) induce temporally modulated responses that are mutually correlated, and that are uncorrelated from those of other sources in the mixture. This "temporal coherence" hypothesis asserts that listening attentively to one or a subset of attributes of a target source enhances their neural responses and concomitantly enhances all other coherent responses, thus binding them together while simultaneously suppressing the incoherent responses to the background features. Here we report on EEG measurements in human subjects engaged in various sound segregation tasks that demonstrate rapid binding among the temporally coherent features of the attended source regardless of their identity, harmonic relationship, or frequency separation, thus confirming the key role temporal coherence plays in the organization of auditory scenes.

neuroscience↗

bioRxiv2020

Distinct higher-order representations of natural sounds in human and ferret auditory cortex

Little is known about how neural representations of natural sounds differ across species. For example, speech and music play a unique role in human hearing, yet it is unclear how auditory representations of speech and music differ between humans and other animals. Using functional Ultrasound imaging, we measured responses in ferrets to a set of natural and spectrotemporally-matched synthetic sounds previously tested in humans. Ferrets showed similar lower-level frequency and modulation tuning to that observed in humans. But while humans showed prominent selectivity for natural vs. synthetic speech and music in non-primary regions, ferret responses to natural and synthetic sounds were closely matched throughout primary and non-primary auditory cortex, even when tested with ferret vocalizations. This finding reveals that auditory representations in humans and ferrets diverge sharply at late stages of cortical processing, potentially driven by higher-order processing demands in speech and music.

neuroscience↗

bioRxiv2020

Neural representation of linguistic feature hierarchy reflects second-language proficiency

Acquiring a new language requires a simultaneous and gradual learning of multiple levels of linguistic attributes. Here, we investigated how this process changes the neural encoding of natural speech by assessing the encoding of the linguistic feature hierarchy in second-language listeners. Electroencephalography (EEG) signals were recorded during English story listening from native Mandarin speakers with varied English proficiency and from native English speakers. We measured the temporal response functions (TRF) for acoustic, phonemic, phonotactic, and semantic features in individual participants and found a main effect of proficiency on the linguistic encoding. This effect of second-language proficiency was particularly prominent on the neural encoding of phonemes, showing stronger encoding of "new" phonemic contrasts (i.e. English contrasts that do not exist in Mandarin) with increasing proficiency. Overall, we found that linguistic feature representation in nonnative listeners progressively converged to that of native listeners with proficiency, which enabled accurate decoding of language proficiency. This detailed view advances our understanding of the cortical processing of linguistic information in second-language learners and provides an objective measure of language proficiency.

neuroscience↗

bioRxiv2019

Cortical encoding of melodic expectations in human temporal cortex

Humans engagement in music rests on underlying elements such as the listeners cultural background and general interest in music, all shaping the way music is processed in the brain and perceived. Crucially, these factors modulate how listeners anticipate musical events, a process inducing instantaneous neural responses as the music confronts these expectations. Measuring such neural correlates would represent a direct window into high-level brain processing of music. Here we recorded electroencephalographic and electrocorticographic brain responses as participants listened to Bach melodies. We assessed the relative contributions of the acoustic versus melodic components of the music to the neural signal. Acoustic features included envelope and its derivative. Melodic features included information on melodic progressions (pitch) and their tempo (onsets), which were extracted from a Markov model predicting the next note based on a corpus of Western music and the preceding proximal musical context. We related the music to brain activity with a linear temporal response function, and demonstrated that cortical responses to music encode melodic expectations. Specifically, individual-subject neural signals were better predicted by a combination of acoustic and melodic expectation features than by either alone. This effect was most pronounced at response latencies up to 350ms, and in both planum temporale and Heschls gyrus. Finally, expectations of pitch and onset-time of musical notes exerted independent cortical effects, and such influences were modulated by the listeners musical expertise. Overall, this study demonstrates how the interplay of experimental and theoretical approaches can yield novel insights into the cortical encoding of melodic expectations.

neuroscience↗

bioRxiv2018

Laminar profile of task-related plasticity in ferret primary auditory cortex

Rapid task-related plasticity is a neural correlate of selective attention in primary auditory cortex (A1). Top-down feedback from higher-order cortex may drive task-related plasticity in A1, characterized by enhanced neural representation of behaviorally meaningful sounds during auditory task performance. Since intracortical connectivity is greater within A1 layers 2/3 (L2/3) than in layers 4-6 (L4-6), we hypothesized that enhanced representation of behaviorally meaningful sounds might be greater in A1 L2/3 than L4-6. To test this hypothesis and study the laminar profile of task-related plasticity, we trained 2 ferrets to detect pure tones while we recorded laminar activity across a 1.8 mm depth in A1. In each experiment, we analyzed current-source densities (CSDs), high-gamma local field potentials (LFPs), and multi-unit spiking in response to identical acoustic stimuli during both passive listening and active task performance. We found that neural responses to auditory targets were enhanced during task performance, and target enhancement was greater in L2/3 than in L4-6. Spectrotemporal receptive fields (STRFs) computed from CSDs, high-gamma LFPs, and multi-unit spiking showed similar increases in auditory target selectivity, also greatest in L2/3. Our results suggest that activity within intracortical networks plays a key role in shaping the underlying neural mechanisms of selective attention.

neuroscience↗

bioRxiv2018

Multi-scale mapping along the auditory hierarchy using high-resolution functional UltraSound in the awake ferret

A major challenge in neuroscience is to longitudinally monitor whole brain activity across multiple spatial scales in the same animal. Functional UltraSound (fUS) is an emerging technology that offers images of cerebral blood volume over large brain portions. Here we show for the first time its capability to resolve the functional organization of sensory systems at multiple scales in awake animals, both within structures by precisely mapping sensory responses, and between structures by elucidating the connectivity scheme of top-down projections. We demonstrate that fUS provides stable (over days), yet rapid, highly-resolved 3D tonotopic maps in the auditory pathway of awake ferrets, with unprecedented sharp functional resolution (100m). This was performed in four different brain regions, including small (1-2mm3 size), subcortical (8mm deep) and previously undescribed structures in the ferret. Furthermore, we used fUS to map longdistance projections from frontal cortex, a key source of sensory response modulation, to auditory cortex.

neuroscience↗

bioRxiv2017

Task Engagement Enhances Population Encoding of Stimulus Meaning in Primary Auditory Cortex

The main functions of primary sensory cortical areas are classically considered to be the extraction and representation of stimulus features. In contrast, higher cortical sensory association areas are thought to be responsible for combining these sensory representations with internal motivations and learnt associations. These regions generate appropriate neural responses that are maintained until a motor command is executed. Within this framework, responses of the primary sensory areas during task performance are expected to carry less information about the behavioral meaning of the stimulus than higher sensory, association, motor and frontal cortices. Here we demonstrate instead that the neuronal population responses in the early primary auditory cortex (A1) display many aspects of responses generally associated with higher-level areas. A1 activity was recorded in awake ferrets while they were either passively listening or actively discriminating two periodic click trains of different rates in a Go/No-Go paradigm. By applying population-level dimensionality reduction techniques, we found that task-engagement induced a shift in the nature of the encoding from a sensory-driven representation of the two stimuli to a behaviorally relevant representation of the two categories that specifically enhances the target stimulus. We demonstrate that this shift in encoding relies partly on a novel mechanism of change in spontaneous activity patterns upon engagement in the task. We show that this population-level representation of stimuli in A1 population activity bears strong similarities to responses in the frontal cortex, but appears earlier following stimulus presentation. Analysis of neural activity recorded in various Go/No-Go tasks, with different sounds and reinforcement paradigms, reveals that this striking population-level enhancement of target representation is a general property of task engagement. These findings indicate that primary sensory cortices play a highly flexible role in the processing of incoming stimuli and implement a crucial change in the structure of population activity in order to extract task-relevant information during behavior.

neuroscience↗