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1.
J Neurosci ; 44(23)2024 Jun 05.
Artigo em Inglês | MEDLINE | ID: mdl-38627089

RESUMO

According to the predictive processing framework, perception emerges from the reciprocal exchange of predictions and prediction errors (PEs) between hierarchically organized neural circuits. The nonlemniscal division of the inferior colliculus (IC) is the earliest source of auditory PE signals, but their neuronal generators, properties, and functional relevance have remained mostly undefined. We recorded single-unit mismatch responses to auditory oddball stimulation at different intensities, together with activity evoked by two sequences of alternating tones to control frequency-specific effects. Our results reveal a differential treatment of the unpredictable "many-standards" control and the predictable "cascade" control by lemniscal and nonlemniscal IC neurons that is not present in the auditory thalamus or cortex. Furthermore, we found that frequency response areas of nonlemniscal IC neurons reflect their role in subcortical predictive processing, distinguishing three hierarchical levels: (1) nonlemniscal neurons with sharply tuned receptive fields exhibit mild repetition suppression without signaling PEs, thereby constituting the input level of the local predictive processing circuitry. (2) Neurons with broadly tuned receptive fields form the main, "spectral" PE signaling system, which provides dynamic gain compensation to near-threshold unexpected sounds. This early enhancement of saliency reliant on spectral features was not observed in the auditory thalamus or cortex. (3) Untuned neurons form an accessory, "nonspectral" PE signaling system, which reports all surprising auditory deviances in a robust and consistent manner, resembling nonlemniscal neurons in the auditory cortex. These nonlemniscal IC neurons show unstructured and unstable receptive fields that could result from inhibitory input controlled by corticofugal projections conveying top-down predictions.


Assuntos
Estimulação Acústica , Percepção Auditiva , Colículos Inferiores , Colículos Inferiores/fisiologia , Animais , Estimulação Acústica/métodos , Masculino , Percepção Auditiva/fisiologia , Neurônios/fisiologia , Feminino , Vias Auditivas/fisiologia , Potenciais Evocados Auditivos/fisiologia , Macaca mulatta
2.
PLoS Biol ; 18(12): e3001019, 2020 12.
Artigo em Inglês | MEDLINE | ID: mdl-33347436

RESUMO

The mismatch negativity (MMN) is a key biomarker of automatic deviance detection thought to emerge from 2 cortical sources. First, the auditory cortex (AC) encodes spectral regularities and reports frequency-specific deviances. Then, more abstract representations in the prefrontal cortex (PFC) allow to detect contextual changes of potential behavioral relevance. However, the precise location and time asynchronies between neuronal correlates underlying this frontotemporal network remain unclear and elusive. Our study presented auditory oddball paradigms along with "no-repetition" controls to record mismatch responses in neuronal spiking activity and local field potentials at the rat medial PFC. Whereas mismatch responses in the auditory system are mainly induced by stimulus-dependent effects, we found that auditory responsiveness in the PFC was driven by unpredictability, yielding context-dependent, comparatively delayed, more robust and longer-lasting mismatch responses mostly comprised of prediction error signaling activity. This characteristically different composition discarded that mismatch responses in the PFC could be simply inherited or amplified downstream from the auditory system. Conversely, it is more plausible for the PFC to exert top-down influences on the AC, since the PFC exhibited flexible and potent predictive processing, capable of suppressing redundant input more efficiently than the AC. Remarkably, the time course of the mismatch responses we observed in the spiking activity and local field potentials of the AC and the PFC combined coincided with the time course of the large-scale MMN-like signals reported in the rat brain, thereby linking the microscopic, mesoscopic, and macroscopic levels of automatic deviance detection.


Assuntos
Córtex Auditivo/fisiologia , Potenciais Evocados Auditivos/fisiologia , Córtex Pré-Frontal/fisiologia , Estimulação Acústica , Animais , Córtex Auditivo/metabolismo , Percepção Auditiva/fisiologia , Eletroencefalografia/métodos , Feminino , Neurônios/fisiologia , Córtex Pré-Frontal/metabolismo , Ratos , Ratos Long-Evans , Tempo de Reação/fisiologia
3.
PLoS Biol ; 18(6): e3000744, 2020 06.
Artigo em Inglês | MEDLINE | ID: mdl-32559190

RESUMO

Dopamine guides behavior and learning through pleasure, according to classic understanding. Dopaminergic neurons are traditionally thought to signal positive or negative prediction errors (PEs) when reward expectations are, respectively, exceeded or not matched. These signed PEs are quite different from the unsigned PEs, which report surprise during sensory processing. But mounting theoretical accounts from the predictive processing framework postulate that dopamine, as a neuromodulator, could potentially regulate the postsynaptic gain of sensory neurons, thereby scaling unsigned PEs according to their expected precision or confidence. Despite ample modeling work, the physiological effects of dopamine on the processing of surprising sensory information are yet to be addressed experimentally. In this study, we tested how dopamine modulates midbrain processing of unexpected tones. We recorded extracellular responses from the rat inferior colliculus to oddball and cascade sequences, before, during, and after the microiontophoretic application of dopamine or eticlopride (a D2-like receptor antagonist). Results demonstrate that dopamine reduces the net neuronal responsiveness exclusively to unexpected sensory input without significantly altering the processing of expected input. We conclude that dopaminergic projections from the thalamic subparafascicular nucleus to the inferior colliculus could encode the expected precision of unsigned PEs, attenuating via D2-like receptors the postsynaptic gain of sensory inputs forwarded by the auditory midbrain neurons. This direct dopaminergic modulation of sensory PE signaling has profound implications for both the predictive coding framework and the understanding of dopamine function.


Assuntos
Córtex Cerebral/fisiologia , Dopamina/farmacologia , Som , Estimulação Acústica , Adaptação Fisiológica , Animais , Córtex Cerebral/efeitos dos fármacos , Feminino , Ratos Long-Evans , Salicilamidas/farmacologia , Tálamo/fisiologia
4.
Hear Res ; 399: 107997, 2021 01.
Artigo em Inglês | MEDLINE | ID: mdl-32482383

RESUMO

Auditory deviance detection is a function of the auditory system that allows reduction of the processing demand for repetitive stimuli while stressing unpredictable ones, which are potentially more informative. Deviance detection has been extensively studied in humans using the oddball paradigm, which evokes an event-related potential known as mismatch negativity (MMN). The same stimulation paradigms are used in animal studies that aim to elucidate the neuronal mechanisms underlying deviance detection. In order to understand the circuitry responsible for deviance detection in the auditory cortex (AC), it is necessary to determine the properties of excitatory and inhibitory neurons separately. Measuring the spike widths of neurons recorded extracellularly from the anaesthetized rat AC, we classified them as fast spiking or regular spiking units. These two neuron types are generally considered as putative inhibitory or excitatory, respectively. In response to an oddball paradigm, we found that both types of units showed similar amounts of deviance detection overall. When considering each AC field separately, we found that only in A1 fast spiking neurons showed higher deviance detection levels than regular spiking neurons, while in the rest of the fields there was no such distinction. Interpreting these responses in the context of the predictive coding framework, we found that the responses of both types of units reflect mainly prediction error signaling (i.e., genuine deviance detection) rather than repetition suppression.


Assuntos
Córtex Auditivo , Estimulação Acústica , Animais , Eletroencefalografia , Potenciais Evocados Auditivos , Ratos , Tempo de Reação
5.
Trends Hear ; 22: 2331216518784822, 2018.
Artigo em Inglês | MEDLINE | ID: mdl-30022729

RESUMO

In this review, we attempt to integrate the empirical evidence regarding stimulus-specific adaptation (SSA) and mismatch negativity (MMN) under a predictive coding perspective (also known as Bayesian or hierarchical-inference model). We propose a renewed methodology for SSA study, which enables a further decomposition of deviance detection into repetition suppression and prediction error, thanks to the use of two controls previously introduced in MMN research: the many-standards and the cascade sequences. Focusing on data obtained with cellular recordings, we explain how deviance detection and prediction error are generated throughout hierarchical levels of processing, following two vectors of increasing computational complexity and abstraction along the auditory neuraxis: from subcortical toward cortical stations and from lemniscal toward nonlemniscal divisions. Then, we delve into the particular characteristics and contributions of subcortical and cortical structures to this generative mechanism of hierarchical inference, analyzing what is known about the role of neuromodulation and local microcircuitry in the emergence of mismatch signals. Finally, we describe how SSA and MMN are occurring at similar time frame and cortical locations, and both are affected by the manipulation of N-methyl- D-aspartate receptors. We conclude that there is enough empirical evidence to consider SSA and MMN, respectively, as the microscopic and macroscopic manifestations of the same physiological mechanism of deviance detection in the auditory cortex. Hence, the development of a common theoretical framework for SSA and MMN is all the more recommendable for future studies. In this regard, we suggest a shared nomenclature based on the predictive coding interpretation of deviance detection.


Assuntos
Estimulação Acústica , Adaptação Fisiológica , Córtex Auditivo/fisiologia , Vias Auditivas , Teorema de Bayes , Eletroencefalografia , Humanos , Neurônios
6.
Nat Commun ; 8(1): 2148, 2017 12 15.
Artigo em Inglês | MEDLINE | ID: mdl-29247159

RESUMO

Perception is characterized by a reciprocal exchange of predictions and prediction error signals between neural regions. However, the relationship between such sensory mismatch responses and hierarchical predictive processing has not yet been demonstrated at the neuronal level in the auditory pathway. We recorded single-neuron activity from different auditory centers in anaesthetized rats and awake mice while animals were played a sequence of sounds, designed to separate the responses due to prediction error from those due to adaptation effects. Here we report that prediction error is organized hierarchically along the central auditory pathway. These prediction error signals are detectable in subcortical regions and increase as the signals move towards auditory cortex, which in turn demonstrates a large-scale mismatch potential. Finally, the predictive activity of single auditory neurons underlies automatic deviance detection at subcortical levels of processing. These results demonstrate that prediction error is a fundamental component of singly auditory neuron responses.

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