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Boubenec, Y.

Publications and source records attributed to Boubenec, Y..

15 recordsLinked to original sources

Neural networks as decision trees: an analytical framework for learning and neural selectivity

Nonlinear neural networks develop structured internal representations, yet how their geometry is determined by the tasks being learned remains poorly understood. Here, we develop an analytical framework for piecewise-linear feedforward and recurrent networks that links learning, activation-region structure, and neural selectivity. We show that, at any stationary point of gradient-aligned learning, a nonlinear network decomposes into local linear regressions over its activation regions. Deviations from the corresponding least-squares solutions are jointly constrained by network weights shared across regions and vanish in the low-error regime, yielding an approximate piecewise least-squares decomposition of the task. This structure admits a decision-tree interpretation, which we recover numerically by fitting trees to predict network activation patterns from the input. We further derive how the regions in which neurons are active determine the task statistics they capture, thereby organizing neural selectivity into distinct subpopulations. The resulting predictions closely match the selectivity geometry observed in simulated networks and two empirical neural datasets. Finally, we show that neural baseline regulates activation pattern diversity, placing networks along a continuum between coarse, generalizing representations and fine-grained, expressive representations. Together, these results establish activation regions as a unifying framework for describing how nonlinear networks decompose task structure into local computations and how those computations can be revealed through neural activity.

neuroscience↗

Sound-evoked facial motion in ferrets: evidence for species differences in sensorimotor coupling

Sensory stimuli elicit uninstructed movements in the mouse, and cortical activity covaries with these movements, raising the question of how much apparent sensory encoding reflects behaviorally driven signals. Still, whether sounds systematically elicit uninstructed movements in non-rodent species is an open question. Here we characterize sound-evoked facial motion and pupil dynamics in head-fixed ferrets, a carnivore species, passively exposed to broadband, natural, and synthetic auditory stimuli. Ferrets reliably produced facial responses to sounds, but unlike mice, these responses were dominated by a single onset-locked component scaling with sound loudness, tracked only temporal modulations below 2 Hz, and carried no information about sound identity or category. Paradoxically, synthetic sounds, which preserved spectrotemporal statistics but lacked higher-order natural structure, elicited stronger responses than their natural counterparts for several sound categories, suggesting that ferret behavioral responses reflect selective sensitivity to acoustic novelty rather than ecological salience. Pupil dynamics mirrored facial motion, consistent with a shared arousal mechanism. Together, these results show that sound-evoked facial motion in ferrets is less stimulus-specific than in mice, and suggest that the tight sensorimotor integration observed in rodents may reflect a species-specific organization rather than a general mammalian principle.

animal behavior and cognition↗

Encoding and combining naturalistic motion cues in the ferret higher visual cortex

Natural visual scenes contain rich flows of pattern motion that vary not only in orientation but also in spatial sizes and temporal rhythms. To properly interpret the motion, the brain must extract individual features and integrate them into coherent parts, and sometimes also segregate these parts from each other. Here, we performed single-neuron recordings in the motion-sensitive higher-order visual cortex (PMLS) of awake ferrets to investigate how complex motion signals are encoded and combined. We presented motion clouds--naturalistic stimuli with parametrically controlled spatiotemporal frequency content--and found that motion features were encoded in a temporally ordered sequence: orientation and spatial frequency emerged within 120 ms after stimulus onset, while temporal frequency and direction followed at later latencies. Time-resolved decoding revealed that this selectivity evolved dynamically within neurons and was distributed across the population. To probe motion integration, we introduced compound motion clouds composed of two or three localized frequency components. Neuronal responses were well explained by a linear pooling model, suggesting a simple summation mechanism of the individual components. However, a distinct subset of neurons exhibited late responses sensitive to changes in speed content despite matched marginals, consistent with receptive fields differentiating along the speed gradient. Together, we have uncovered a structured and distributed code for motion in high-level visual cortex, and provide mechanistic insights into how the brain parses complex motion in natural scenes.

neuroscience↗

Sensorimotor remapping drives task specialization in prefrontal cortex

The prefrontal cortex (PFC) plays a key role in flexible, context-dependent decision-making. Yet, the population-level mechanisms that support this flexibility remain unclear: is there a generalist neural population involved in representing useful information across tasks, or are representations distributed over multiple modules of task-specialized subpopulations? Here, we investigate whether the population structure modularity in medial prefrontal cortex (mPFC) increases with sensorimotor remapping between task rules in two different paradigms. In a paradigm where all stimuli were remapped, we found a highly modular structure with two task-specialized subpopulations and one generalist. In a different paradigm where only half of the stimuli were remapped, modularity decreased but remained significant. Based on predictions drawn from a recurrent neural network fitted to experimental data, we propose that a gain modulation by global inhibition of mPFC can explain how task-specialized neurons emerge to varying degrees in each paradigm.

neuroscience↗

Hierarchical encoding of natural sounds mixtures in ferret auditory cortex

Extracting relevant auditory signals from complex natural scenes is a fundamental challenge for the auditory system. Sounds from multiple sources overlap in time and frequency. In particular, dynamic "foreground" sounds are often masked by more stationary "background" sounds. Human auditory cortex exhibits a hierarchical organization where background-invariant representations are progressively enhanced along the processing stream, from primary to non-primary regions. However, we do not know whether this organizational principle is conserved across species and which neural mechanisms drive this invariance. To address these questions, we investigated background invariance in ferret auditory cortex using functional ultrasound imaging (fUSI), which enables large-scale, high-resolution recordings of hemodynamic responses. We measured responses across primary, secondary, and tertiary auditory cortical regions as ferrets passively listened to mixtures of natural sounds and their components in isolation. We found a hierarchical gradient of background invariance, mirroring findings in humans: responses in primary auditory cortex reflected contributions from both foreground and background sounds, while background invariance increased in higher-order auditory regions. Using a spectrotemporal filter-bank model, we found that in ferrets, this hierarchical structure could be largely explained by tuning to low-order acoustic features. However, this model failed to fully account for background invariance in human non-primary auditory cortex, suggesting that additional, higher-order mechanisms are crucial for background segregation in humans.

neuroscience↗

Neurons in auditory cortex integrate information within constrained temporal windows that are invariant to the stimulus context and information rate

Much remains unknown about the computations that allow animals to flexibly integrate across multiple timescales in natural sounds. One key question is whether multiscale integration is accomplished by diverse populations of neurons, each of which integrates information within a constrained temporal window, or whether individual units effectively integrate across many different temporal scales depending on the information rate. Here, we show that responses from neurons throughout the ferret auditory cortex are nearly completely unaffected by sounds falling beyond a time-limited "integration window". This window varies substantially across cells within the auditory cortex ([~]15 to [~]150 ms), increasing substantially from primary to non-primary auditory cortex across all cortical layers, but is unaffected by the information rate of sound. These results indicate that multiscale computation is predominantly accomplished by diverse and hierarchically organized neural populations, each of which integrates information within a highly constrained temporal window.

neuroscience↗

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↗

Algebraic structures emerge from the self-supervised learning of natural sounds.

Humans can spontaneously detect complex algebraic structures. Historically, two opposing views explain this ability, at the root of language and music acquisition. Some argue for the existence of an innate and specific mechanism, like "merge" (Chomsky) or "neural recursion" (Dehaene). Others argue that this ability emerges from experience (e.g. Bates): i.e. when generic learning principles continuously process sensory inputs. These two views, however, remain difficult to test experimentally. Here, we use deep learning models to evaluate the factors that lead to the spontaneous detection of algebraic structures in the auditory modality. Specifically, we train multiple deep learning models with a variable amount of natural sounds and a self-supervised learning objective. We then expose these models to the experimental paradigms classically used to evaluate the processing of algebraic structures. Like humans, these models spontaneously detect repeated sequences, probabilistic chunks and complex algebraic structures. Also like humans, this ability diminishes with structure complexity. Importantly, this ability can emerge from experience alone: the more the models are exposed to natural sounds, the more they spontaneously detect increasingly complex structures. Finally, this ability does not emerge in models pretrained only on speech, and emerges more rapidly in models pretrained with music than environmental sounds. Overall, our study provides an operational framework to clarify sufficient built-in and acquired principles that model humans advanced capacity to detect algebraic structures in sounds. Significance StatementExperimentalists have repeatedly observed a human advantage in the detection of algebraic structures, notably through auditory paradigms. This ability to detect structure is thought to be key to the emergence of complex cognitive operations. Yet, it remains debated if this ability is discovered or innate in the form of a specific mechanism. In this article, the authors show how a model progressively and spontaneously learns to detect auditory structure. The model replicate several experimental findings but only under certain developmental conditions. Notably, exposition to music or environmental sounds, but not speech, is sufficient for the emergence of algebraic structure detection. As a result, this work proposes self-supervised learning as a developmental model of abstract cognitive abilities.

neuroscience↗

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↗

Flexible selection of task-relevant features through across-area population gating

Brains can gracefully weed out irrelevant stimuli to guide behavior. This feat is believed to rely on a progressive selection of task-relevant stimuli across the cortical hierarchy, but the specific across-area interactions enabling stimulus selection are still unclear. Here, we propose that population gating, occurring within A1 but controlled by top-down inputs from mPFC, can support across-area stimulus selection. Examining single-unit activity recorded while rats performed an auditory context-dependent task, we found that A1 encoded relevant and irrelevant stimuli along a common dimension of its neural space. Yet, the relevant stimulus encoding was enhanced along an extra dimension. In turn, mPFC encoded only the stimulus relevant to the ongoing context. To identify candidate mechanisms for stimulus selection within A1, we reverse-engineered low-rank RNNs trained on a similar task. Our analyses predicted that two context-modulated neural populations gated their preferred stimulus in opposite contexts, which we confirmed in further analyses of A1. Finally, we show in a two-region RNN how population gating within A1 could be controlled by top-down inputs from PFC, enabling flexible across-area communication despite fixed inter-areal connectivity.

neuroscience↗

Hidden temporal structure of the ongoing task impacts detection strategy and is reflected in pupillary dynamics

Estimating temporal regularities in incoming sensory inputs supports optimal decisions in noisy environments. In particular, inferred temporal structure can ease the detection of likely target events. Here we postulated that timely urgency signals can adapt subjects decision-making to the ongoing task temporal structure, possibly through neuromodulatory tone. To test this hypothesis, we used an auditory change detection task in which targets followed a block-based temporal contingency, unbeknownst to participants. False alarm occurrences were driven by the distribution of target timings, indicating that participants adapted their behavior to the ongoing temporal structure. Task-evoked pupillary responses were larger for blocks with earliest target timings, and correlated with individual subjects behavioral adaptation. Individual pupil responses matched an urgency signal extracted from a decision model fitted to behavior. This work demonstrates that internal temporal expectation can be tracked through pupillary dynamics, suggesting a role of neuromodulatory systems in context-dependent modulation of decision variable dynamics.

neuroscience↗

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↗

Dissociating task acquisition from expression during learning reveals latent knowledge

Performance on cognitive tasks during learning is used to measure intelligence, yet it remains controversial since such testing is susceptible to contextual factors. To what extent does performance during learning depend on the testing context, rather than underlying knowledge? We trained mice, rats and ferrets on a range of tasks to examine how testing context impacts the acquisition of knowledge versus its expression. We interleaved reinforced trials with \"probe\" trials in which we omitted reinforcement. Across tasks, each animal species performed remarkably better in probe trials during learning and inter-animal variability was strikingly reduced. Reinforcement feedback is thus critical for learning-related plasticity but, paradoxically, masks the expression of underlying knowledge. We capture these results with a network model in which learning occurs during reinforced trials while context modulates only the read-out parameters. Probing learning by omitting reinforcement thus uncovers latent knowledge and identifies context--not \"smartness\"--as the major source of individual variability.\n\nHIGHLIGHTSO_LIKnowledge acquisition and expression can be segregated by the introduction of non-reinforced probe trials across a variety of animal species and behavioral tasks.\nC_LIO_LIAnimals learn much faster and in a more stereotyped way in non-reinforced probe trials than their performance in the presence of reinforcement suggests.\nC_LIO_LIUnderperformance and variability in performance arise from sensitivity to the behavioral testing context, not acquisition of sensorimotor associations.\nC_LIO_LIA circuit model accounts for context-dependent performance by modulating the integration of sensorimotor associations.\nC_LI\n\neTOCKuchibhotla et al. show the acquisition and expression of knowledge can be behaviorally dissociated in mice, rats, and ferrets across a variety of sensorimotor tasks. Across animals, variability in performance arises from the testing context, not underlying aptitude.

neuroscience↗

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↗

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↗