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Experience-driven development of decision-related representations in the auditory cortex

ABSTRACT: Associating sensory stimuli with behavioral significance induces substantial changes in stimulus representations. Recent studies suggest that primary sensory cortices not only adjust representations of task-relevant stimuli, but actively participate in encoding decision-making features. We sought to determine whether this trait is innate in sensory cortices or if choice representation develops with time and experience. To trace choice representation development, we perform chronic two-photon calcium imaging in the primary auditory cortex of head-fixed mice while they gain experience in a tone detection task with a delayed decision window. Our results reveal a progressive increase in choice-dependent activity within a specific subpopulation of neurons, aligning with growing task familiarity and adapting to changing task rules. Task experience correlates with heightened synchronized activity in these populations and the ability to differentiate between different types of behavioral decisions. Notably, the activity of this subpopulation accurately decodes the same action at different task phases. Our findings establish a dynamic restructuring of population activity in the auditory cortex to encode decision-making features that develop over time and refines with experience.

SUBMITTER: Dr. Jennifer Resnik

PROVIDER: S-SCDT-10_1038-S44319-024-00309-0 | biostudies-other |

REPOSITORIES: biostudies-other

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Source data: Experience-driven development of decision-related representations in the auditory cortex

Project description: Not available

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Project description:Animals require the ability to ignore sensory stimuli that have no consequence yet respond to the same stimuli when they become useful. However, the brain circuits that govern this flexibility in sensory processing are not well understood. Here we show in mouse primary auditory cortex (A1) that daily passive sound exposure causes a long-lasting reduction in representations of the experienced sound by layer 2/3 pyramidal cells. This habituation arises locally in A1 and involves an enhancement in inhibition and selective upregulation in the activity of somatostatin-expressing inhibitory neurons (SOM cells). Furthermore, when mice engage in sound-guided behavior, pyramidal cell excitatory responses to habituated sounds are enhanced, whereas SOM cell responses are diminished. Together, our results demonstrate the bidirectional modulation of A1 sensory representations and suggest that SOM cells gate cortical information flow based on the behavioral relevance of the stimulus.

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Project description:A key function of the brain is to provide a stable representation of an object's location in the world. In hearing, sound azimuth and elevation are encoded by neurons throughout the auditory system, and auditory cortex is necessary for sound localization. However, the coordinate frame in which neurons represent sound space remains undefined: classical spatial receptive fields in head-fixed subjects can be explained either by sensitivity to sound source location relative to the head (egocentric) or relative to the world (allocentric encoding). This coordinate frame ambiguity can be resolved by studying freely moving subjects; here we recorded spatial receptive fields in the auditory cortex of freely moving ferrets. We found that most spatially tuned neurons represented sound source location relative to the head across changes in head position and direction. In addition, we also recorded a small number of neurons in which sound location was represented in a world-centered coordinate frame. We used measurements of spatial tuning across changes in head position and direction to explore the influence of sound source distance and speed of head movement on auditory cortical activity and spatial tuning. Modulation depth of spatial tuning increased with distance for egocentric but not allocentric units, whereas, for both populations, modulation was stronger at faster movement speeds. Our findings suggest that early auditory cortex primarily represents sound source location relative to ourselves but that a minority of cells can represent sound location in the world independent of our own position.

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Auditory Frequency Representations in Human Somatosensory Cortex.

Project description:Recent studies have challenged the traditional notion of modality-dedicated cortical systems by showing that audition and touch evoke responses in the same sensory brain regions. While much of this work has focused on somatosensory responses in auditory regions, fewer studies have investigated sound responses and representations in somatosensory regions. In this functional magnetic resonance imaging (fMRI) study, we measured BOLD signal changes in participants performing an auditory frequency discrimination task and characterized activation patterns related to stimulus frequency using both univariate and multivariate analysis approaches. Outside of bilateral temporal lobe regions, we observed robust and frequency-specific responses to auditory stimulation in classically defined somatosensory areas. Moreover, using representational similarity analysis to define the relationships between multi-voxel activation patterns for all sound pairs, we found clear similarity patterns for auditory responses in the parietal lobe that correlated significantly with perceptual similarity judgments. Our results demonstrate that auditory frequency representations can be distributed over brain regions traditionally considered to be dedicated to somatosensation. The broad distribution of auditory and tactile responses over parietal and temporal regions reveals a number of candidate brain areas that could support general temporal frequency processing and mediate the extensive and robust perceptual interactions between audition and touch.

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Project description:In many natural environments the value of a choice gradually gets better or worse as circumstances change. Discerning such trends makes predicting future choice values possible. We show that humans track such trends by comparing estimates of recent and past reward rates, which they are able to hold simultaneously in the dorsal anterior cingulate cortex (dACC). Comparison of recent and past reward rates with positive and negative decision weights is reflected by opposing dACC signals indexing these quantities. The relative strengths of time-linked reward representations in dACC predict whether subjects persist in their current behaviour or switch to an alternative. Computationally, trend-guided choice can be modelled by using a reinforcement-learning mechanism that computes a longer-term estimate (or expectation) of prediction errors. Using such a model, we find a relative predominance of expected prediction errors in dACC, instantaneous prediction errors in the ventral striatum and choice signals in the ventromedial prefrontal cortex.

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Project description:The acoustic dimensions that distinguish speech sounds (like the vowel differences in "boot" and "boat") also differentiate speakers' voices. Therefore, listeners must normalize across speakers without losing linguistic information. Past behavioral work suggests an important role for auditory contrast enhancement in normalization: preceding context affects listeners' perception of subsequent speech sounds. Here, using intracranial electrocorticography in humans, we investigate whether and how such context effects arise in auditory cortex. Participants identified speech sounds that were preceded by phrases from two different speakers whose voices differed along the same acoustic dimension as target words (the lowest resonance of the vocal tract). In every participant, target vowels evoke a speaker-dependent neural response that is consistent with the listener's perception, and which follows from a contrast enhancement model. Auditory cortex processing thus displays a critical feature of normalization, allowing listeners to extract meaningful content from the voices of diverse speakers.

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Project description:Iterated ripple noise (IRN) is a type of pitch-evoking stimulus that is commonly used in neuroimaging studies of pitch processing. When contrasted with a spectrally matched Gaussian noise, it is known to produce a consistent response in a region of auditory cortex that includes an area antero-lateral to the primary auditory fields (lateral Heschl's gyrus). The IRN-related response has often been attributed to pitch, although recent evidence suggests that it is more likely driven by slowly varying spectro-temporal modulations not related to pitch. The present functional magnetic resonance imaging (fMRI) study showed that both pitch-related temporal regularity and slow modulations elicited a significantly greater response than a baseline Gaussian noise in an area that has been pre-defined as pitch-responsive. The region was sensitive to both pitch salience and slow modulation salience. The responses to pitch and spectro-temporal modulations interacted in a saturating manner, suggesting that there may be an overlap in the populations of neurons coding these features. However, the interaction may have been influenced by the fact that the two pitch stimuli used (IRN and unresolved harmonic complexes) differed in terms of pitch salience. Finally, the results support previous findings suggesting that the cortical response to IRN is driven in part by slow modulations, not by pitch.

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Neuronal representations of distance in human auditory cortex.

Project description:Neuronal mechanisms of auditory distance perception are poorly understood, largely because contributions of intensity and distance processing are difficult to differentiate. Typically, the received intensity increases when sound sources approach us. However, we can also distinguish between soft-but-nearby and loud-but-distant sounds, indicating that distance processing can also be based on intensity-independent cues. Here, we combined behavioral experiments, fMRI measurements, and computational analyses to identify the neural representation of distance independent of intensity. In a virtual reverberant environment, we simulated sound sources at varying distances (15-100 cm) along the right-side interaural axis. Our acoustic analysis suggested that, of the individual intensity-independent depth cues available for these stimuli, direct-to-reverberant ratio (D/R) is more reliable and robust than interaural level difference (ILD). However, on the basis of our behavioral results, subjects' discrimination performance was more consistent with complex intensity-independent distance representations, combining both available cues, than with representations on the basis of either D/R or ILD individually. fMRI activations to sounds varying in distance (containing all cues, including intensity), compared with activations to sounds varying in intensity only, were significantly increased in the planum temporale and posterior superior temporal gyrus contralateral to the direction of stimulation. This fMRI result suggests that neurons in posterior nonprimary auditory cortices, in or near the areas processing other auditory spatial features, are sensitive to intensity-independent sound properties relevant for auditory distance perception.

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Causal contribution of primate auditory cortex to auditory perceptual decision-making.

Project description:Auditory perceptual decisions are thought to be mediated by the ventral auditory pathway. However, the specific and causal contributions of different brain regions in this pathway, including the middle-lateral (ML) and anterolateral (AL) belt regions of the auditory cortex, to auditory decisions have not been fully identified. To identify these contributions, we recorded from and microstimulated ML and AL sites while monkeys decided whether an auditory stimulus contained more low-frequency or high-frequency tone bursts. Both ML and AL neural activity was modulated by the frequency content of the stimulus. But, only the responses of the most stimulus-sensitive AL neurons were systematically modulated by the monkeys' choices. Consistent with this observation, microstimulation of AL, but not ML, systematically biased the monkeys' behavior toward the choice associated with the preferred frequency of the stimulated site. Together, these findings suggest that AL directly and causally contributes sensory evidence to form this auditory decision.

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Prestimulus influences on auditory perception from sensory representations and decision processes.

Project description:The qualities of perception depend not only on the sensory inputs but also on the brain state before stimulus presentation. Although the collective evidence from neuroimaging studies for a relation between prestimulus state and perception is strong, the interpretation in the context of sensory computations or decision processes has remained difficult. In the auditory system, for example, previous studies have reported a wide range of effects in terms of the perceptually relevant frequency bands and state parameters (phase/power). To dissociate influences of state on earlier sensory representations and higher-level decision processes, we collected behavioral and EEG data in human participants performing two auditory discrimination tasks relying on distinct acoustic features. Using single-trial decoding, we quantified the relation between prestimulus activity, relevant sensory evidence, and choice in different task-relevant EEG components. Within auditory networks, we found that phase had no direct influence on choice, whereas power in task-specific frequency bands affected the encoding of sensory evidence. Within later-activated frontoparietal regions, theta and alpha phase had a direct influence on choice, without involving sensory evidence. These results delineate two consistent mechanisms by which prestimulus activity shapes perception. However, the timescales of the relevant neural activity depend on the specific brain regions engaged by the respective task.

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