RESUMEN
Quantifying the functional relations between the nodes in a network based on local observations is a key challenge in studying complex systems. Most existing time series analysis techniques for this purpose provide static estimates of the network properties, pertain to stationary Gaussian data, or do not take into account the ubiquitous sparsity in the underlying functional networks. When applied to spike recordings from neuronal ensembles undergoing rapid task-dependent dynamics, they thus hinder a precise statistical characterization of the dynamic neuronal functional networks underlying adaptive behavior. We develop a dynamic estimation and inference paradigm for extracting functional neuronal network dynamics in the sense of Granger, by integrating techniques from adaptive filtering, compressed sensing, point process theory, and high-dimensional statistics. We demonstrate the utility of our proposed paradigm through theoretical analysis, algorithm development, and application to synthetic and real data. Application of our techniques to two-photon Ca2+ imaging experiments from the mouse auditory cortex reveals unique features of the functional neuronal network structures underlying spontaneous activity at unprecedented spatiotemporal resolution. Our analysis of simultaneous recordings from the ferret auditory and prefrontal cortical areas suggests evidence for the role of rapid top-down and bottom-up functional dynamics across these areas involved in robust attentive behavior.
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Corteza Auditiva/fisiología , Señalización del Calcio/fisiología , Calcio/metabolismo , Modelos Neurológicos , Red Nerviosa/fisiología , Animales , Corteza Auditiva/diagnóstico por imagen , Ratones , Red Nerviosa/diagnóstico por imagenRESUMEN
"Music As a Coevolved System for Social Bonding" (MSB) is a brilliant synthesis and appealing hypothesis offering insights into the evolution and social bonding of musicality, but is so broad and sweeping it will be challenging to test, prove or falsify in the Popperian sense (Popper, 1959). After general comments, I focus my critique on underlying neurobiological mechanisms, and offer some suggestions for experimental tests of MSB.
Asunto(s)
Música , HumanosRESUMEN
Natural sounds such as vocalizations often have covarying acoustic attributes, resulting in redundancy in neural coding. The efficient coding hypothesis proposes that sensory systems are able to detect such covariation and adapt to reduce redundancy, leading to more efficient neural coding. Recent psychoacoustic studies have shown the auditory system can rapidly adapt to efficiently encode two covarying dimensions as a single dimension, following passive exposure to sounds in which temporal and spectral attributes covaried in a correlated fashion. However, these studies observed a cost to this adaptation, which was a loss of sensitivity to the orthogonal dimension. Here we explore the neural basis of this psychophysical phenomenon by recording single-unit responses from the primary auditory cortex in awake ferrets exposed passively to stimuli with two correlated attributes, similar in stimulus design to the psychoacoustic experiments in humans. We found: (1) the signal-to-noise ratio of spike-rate coding of cortical responses driven by sounds with correlated attributes remained unchanged along the exposure dimension, but was reduced along the orthogonal dimension; (2) performance of a decoder trained with spike data to discriminate stimuli along the orthogonal dimension was equally reduced; (3) correlations between neurons tuned to the two covarying attributes decreased after exposure; and (4) these exposure effects still occurred if sounds were correlated along two acoustic dimensions, but varied randomly along a third dimension. These neurophysiological results are consistent with the efficient coding hypothesis and may help deepen our understanding of how the auditory system encodes and represents acoustic regularities and covariance.SIGNIFICANCE STATEMENT The efficient coding (EC) hypothesis (Attneave, 1954; Barlow, 1961) proposes that the neural code in sensory systems efficiently encodes natural stimuli by minimizing the number of spikes to transmit a sensory signal. Results of recent psychoacoustic studies in humans are consistent with the EC hypothesis in that, following passive exposure to stimuli with correlated attributes, the auditory system rapidly adapts so as to more efficiently encode the two covarying dimensions as a single dimension. In the current neurophysiological experiments, using a similar stimulus design and the experimental paradigm to the psychoacoustic studies of Stilp et al. (2010) and Stilp and Kluender (2011, 2012, 2016), we recorded responses from single neurons in the auditory cortex of the awake ferret, showing adaptive efficient neural coding of two correlated acoustic attributes.
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Adaptación Fisiológica , Corteza Auditiva/fisiología , Percepción Auditiva/fisiología , Neuronas/fisiología , Estimulación Acústica , Potenciales de Acción , Animales , Femenino , Hurones , Modelos Neurológicos , PsicoacústicaRESUMEN
Responses of auditory cortical neurons encode sound features of incoming acoustic stimuli and also are shaped by stimulus context and history. Previous studies of mammalian auditory cortex have reported a variable time course for such contextual effects ranging from milliseconds to minutes. However, in secondary auditory forebrain areas of songbirds, long-term stimulus-specific neuronal habituation to acoustic stimuli can persist for much longer periods of time, ranging from hours to days. Such long-term habituation in the songbird is a form of long-term auditory memory that requires gene expression. Although such long-term habituation has been demonstrated in avian auditory forebrain, this phenomenon has not previously been described in the mammalian auditory system. Utilizing a similar version of the avian habituation paradigm, we explored whether such long-term effects of stimulus history also occur in auditory cortex of a mammalian auditory generalist, the ferret. Following repetitive presentation of novel complex sounds, we observed significant response habituation in secondary auditory cortex, but not in primary auditory cortex. This long-term habituation appeared to be independent for each novel stimulus and often lasted for at least 20 min. These effects could not be explained by simple neuronal fatigue in the auditory pathway, because time-reversed sounds induced undiminished responses similar to those elicited by completely novel sounds. A parallel set of pupillometric response measurements in the ferret revealed long-term habituation effects similar to observed long-term neural habituation, supporting the hypothesis that habituation to passively presented stimuli is correlated with implicit learning and long-term recognition of familiar sounds.SIGNIFICANCE STATEMENT Long-term habituation in higher areas of songbird auditory forebrain is associated with gene expression and is correlated with recognition memory. Similar long-term auditory habituation in mammals has not been previously described. We studied such habituation in single neurons in the auditory cortex of awake ferrets that were passively listening to repeated presentations of various complex sounds. Responses exhibited long-lasting habituation (at least 20 min) in the secondary, but not primary auditory cortex. Habituation ceased when stimuli were played backward, despite having identical spectral content to the original sound. This long-term neural habituation correlated with similar habituation of ferret pupillary responses to repeated presentations of the same stimuli, suggesting that stimulus habituation is retained as a long-term behavioral memory.
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Estimulación Acústica/métodos , Corteza Auditiva/fisiología , Percepción Auditiva/fisiología , Habituación Psicofisiológica/fisiología , Memoria/fisiología , Animales , Vías Auditivas/fisiología , Femenino , HuronesRESUMEN
Sensory environments change over a wide dynamic range and sensory processing can change rapidly to facilitate stable perception. While rapid changes may occur throughout the sensory processing pathway, cortical changes are believed to profoundly influence perception. Prior stimulation studies showed that orbitofrontal cortex (OFC) can modify receptive fields and sensory coding in A1, but the engagement of OFC during listening and the pathways mediating OFC influences on A1 are unknown. We show in mice that OFC neurons respond to sounds consistent with a role of OFC in audition. We then show in vitro that OFC axons are present in A1 and excite pyramidal and GABAergic cells in all layers of A1 via glutamatergic synapses. Optogenetic stimulation of OFC terminals in A1 in vivo evokes short-latency neural activity in A1 and pairing activation of OFC projections in A1 with sounds alters sound-evoked A1 responses. Together, our results identify a direct connection from OFC to A1 that can excite A1 neurons at the earliest stage of cortical processing, and thereby sculpt A1 receptive fields. These results are consistent with a role for OFC in adjusting to changing behavioral relevance of sensory inputs and modulating A1 receptive fields to enhance sound processing.
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Corteza Auditiva/citología , Red Nerviosa/fisiología , Neuronas/fisiología , Corteza Prefrontal/citología , Sonido , Estimulación Acústica , Potenciales de Acción/fisiología , Animales , Percepción Auditiva , Axones/fisiología , Channelrhodopsins/genética , Channelrhodopsins/metabolismo , Potenciales Evocados/fisiología , Potenciales Postsinápticos Excitadores , Femenino , Glutamato Descarboxilasa/genética , Glutamato Descarboxilasa/metabolismo , Proteínas Luminiscentes/genética , Proteínas Luminiscentes/metabolismo , Masculino , Ratones , Ratones Endogámicos C57BL , Tiempo de Reacción/fisiologíaRESUMEN
Humans and animals can reliably perceive behaviorally relevant sounds in noisy and reverberant environments, yet the neural mechanisms behind this phenomenon are largely unknown. To understand how neural circuits represent degraded auditory stimuli with additive and reverberant distortions, we compared single-neuron responses in ferret primary auditory cortex to speech and vocalizations in four conditions: clean, additive white and pink (1/f) noise, and reverberation. Despite substantial distortion, responses of neurons to the vocalization signal remained stable, maintaining the same statistical distribution in all conditions. Stimulus spectrograms reconstructed from population responses to the distorted stimuli resembled more the original clean than the distorted signals. To explore mechanisms contributing to this robustness, we simulated neural responses using several spectrotemporal receptive field models that incorporated either a static nonlinearity or subtractive synaptic depression and multiplicative gain normalization. The static model failed to suppress the distortions. A dynamic model incorporating feed-forward synaptic depression could account for the reduction of additive noise, but only the combined model with feedback gain normalization was able to predict the effects across both additive and reverberant conditions. Thus, both mechanisms can contribute to the abilities of humans and animals to extract relevant sounds in diverse noisy environments.
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Corteza Auditiva/fisiología , Percepción del Habla/fisiología , Estimulación Acústica , Animales , Femenino , Hurones/fisiología , Humanos , Modelos Neurológicos , Neuronas/fisiología , Ruido , Dinámicas no Lineales , Vocalización AnimalRESUMEN
In order to explore the representation of sound features in auditory long-term memory, two groups of ferrets were trained on Go vs Nogo, 3-zone classification tasks. The sound stimuli differed primarily along the spectral and temporal dimensions. In Group 1, two ferrets were trained to (i) classify tones based on their frequency (Tone-task), and subsequently learned to (ii) classify white noise based on its amplitude modulation rate (AM-task). In Group 2, two ferrets were trained to classify tones based on correlated combinations of their frequency and AM rate (AM-Tone task). Both groups of ferrets learned their tasks and were able to generalize performance along the trained spectral (tone frequency) or temporal (AM rate) dimensions. Insights into stimulus representations in memory were gained when the animals were tested with a diverse set of untrained probes that mixed features from the two dimensions. Animals exhibited a complex pattern of responses to the probes reflecting primarily the probes' spectral similarity with the training stimuli, and secondarily the temporal features of the stimuli. These diverse behavioral decisions could be well accounted for by a nearest-neighbor classifier model that relied on a multiscale spectrotemporal cortical representation of the training and probe sounds.
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Memoria a Largo Plazo , Estimulación Acústica , Animales , Corteza Auditiva , Percepción Auditiva , AprendizajeRESUMEN
Complex natural and environmental sounds, such as speech and music, convey information along both spectral and temporal dimensions. The cortical representation of such stimuli rapidly adapts when animals become actively engaged in discriminating them. In this study, we examine the nature of these changes using simplified spectrotemporal versions (upward vs downward shifting tone sequences) with domestic ferrets (Mustela putorius). Cortical processing rapidly adapted to enhance the contrast between the two discriminated stimulus categories, by changing spectrotemporal receptive field properties to encode both the spectral and temporal structure of the tone sequences. Furthermore, the valence of the changes was closely linked to the task reward structure: stimuli associated with negative reward became enhanced relative to those associated with positive reward. These task- and-stimulus-related spectrotemporal receptive field changes occurred only in trained animals during, and immediately following, behavior. This plasticity was independently confirmed by parallel changes in a directionality function measured from the responses to the transition of tone sequences during task performance. The results demonstrate that induced patterns of rapid plasticity reflect closely the spectrotemporal structure of the task stimuli, thus extending the functional relevance of rapid task-related plasticity to the perception and learning of natural sounds such speech and animal vocalizations.
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Adaptación Psicológica/fisiología , Corteza Auditiva/fisiología , Percepción Auditiva/fisiología , Plasticidad Neuronal/fisiología , Estimulación Acústica/métodos , Animales , Aprendizaje Discriminativo/fisiología , Hurones , Tiempo de Reacción/fisiologíaRESUMEN
As sensory stimuli and behavioral demands change, the attentive brain quickly identifies task-relevant stimuli and associates them with appropriate motor responses. The effects of attention on sensory processing vary across task paradigms, suggesting that the brain may use multiple strategies and mechanisms to highlight attended stimuli and link them to motor action. To better understand factors that contribute to these variable effects, we studied sensory representations in primary auditory cortex (A1) during two instrumental tasks that shared the same auditory discrimination but required different behavioral responses, either approach or avoidance. In the approach task, ferrets were rewarded for licking a spout when they heard a target tone amid a sequence of reference noise sounds. In the avoidance task, they were punished unless they inhibited licking to the target. To explore how these changes in task reward structure influenced attention-driven rapid plasticity in A1, we measured changes in sensory neural responses during behavior. Responses to the target changed selectively during both tasks but did so with opposite sign. Despite the differences in sign, both effects were consistent with a general neural coding strategy that maximizes discriminability between sound classes. The dependence of the direction of plasticity on task suggests that representations in A1 change not only to sharpen representations of task-relevant stimuli but also to amplify responses to stimuli that signal aversive outcomes and lead to behavioral inhibition. Thus, top-down control of sensory processing can be shaped by task reward structure in addition to the required sensory discrimination.
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Corteza Auditiva/fisiología , Plasticidad Neuronal/fisiología , Recompensa , Análisis y Desempeño de Tareas , Estimulación Acústica , Animales , Reacción de Prevención/fisiología , Conducta Animal/fisiología , Hurones , Factores de TiempoRESUMEN
In this study, we explored ways to account more accurately for responses of neurons in primary auditory cortex (A1) to natural sounds. The auditory cortex has evolved to extract behaviorally relevant information from complex natural sounds, but most of our understanding of its function is derived from experiments using simple synthetic stimuli. Previous neurophysiological studies have found that existing models, such as the linear spectro-temporal receptive field (STRF), fail to capture the entire functional relationship between natural stimuli and neural responses. To study this problem, we compared STRFs for A1 neurons estimated using a natural stimulus, continuous speech, with STRFs estimated using synthetic ripple noise. For about one-third of the neurons, we found significant differences between STRFs, usually in the temporal dynamics of inhibition and/or overall gain. This shift in tuning resulted primarily from differences in the coarse temporal structure of the speech and noise stimuli. Using simulations, we found that the stimulus dependence of spectro-temporal tuning can be explained by a model in which synaptic inputs to A1 neurons are susceptible to rapid nonlinear depression. This dynamic reshaping of spectro-temporal tuning suggests that synaptic depression may enable efficient encoding of natural auditory stimuli.
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Estimulación Acústica/métodos , Corteza Auditiva/fisiología , Depresión Sináptica a Largo Plazo/fisiología , Sinapsis/fisiología , Potenciales de Acción/fisiología , Animales , Vías Auditivas/fisiología , Percepción Auditiva/fisiología , Femenino , Hurones , Humanos , Masculino , Plasticidad Neuronal/fisiología , Factores de TiempoRESUMEN
The existence of relative pitch perception in animals is difficult to demonstrate, since unlike humans, animals often attend to absolute rather than relative properties of sound elements. However, the results of the present study show that ferrets can be trained using relative pitch to discriminate two-tone sequences (rising vs. falling). Three ferrets were trained using a positive-reinforcement paradigm in which sequences of reference (one to five repeats) and target stimuli were presented, and animals were rewarded only when responding correctly to the target. The training procedure consisted of three training phases that successively shaped the ferrets to attend to relative pitch. In Phase-1 training, animals learned the basic task with sequences of invariant tone-pairs and could use absolute pitch information. During Phase-2 training, in order to emphasize relative cues, absolute pitch was varied each trial within a two-octave frequency range. In Phase-3 training, absolute pitch cues were removed, and only relative cue information was available to solve the task. Two ferrets successfully completed training on all three phases and achieved significant discriminative performance over the trained four-octave frequency range. These results suggest that ferrets can be trained to discern the relative pitch relationship of a sequence of tone-pairs independent of frequency.
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Conducta Animal/fisiología , Condicionamiento Operante/fisiología , Hurones/fisiología , Percepción de la Altura Tonal/fisiología , Estimulación Acústica , Animales , Señales (Psicología) , Aprendizaje Discriminativo/fisiología , FemeninoRESUMEN
The origin of brain mechanisms that support human language-whether these originated de novo in humans or evolved from a neural substrate that existed in a common ancestor-remains a controversial issue. Although the answer is not provided by the fossil record, it is possible to make inferences by studying living species of nonhuman primates. Here we identified neural systems associated with perceiving species-specific vocalizations in rhesus macaques using H(2)(15)O positron emission tomography (PET). These vocalizations evoke distinct patterns of brain activity in homologs of the human perisylvian language areas. Rather than resulting from differences in elementary acoustic properties, this activity seems to reflect higher order auditory processing. Although parallel evolution within independent primate species is feasible, this finding suggests the possibility that the last common ancestor of macaques and humans, which lived 25-30 million years ago, possessed key neural mechanisms that were plausible candidates for exaptation during the evolution of language.
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Percepción Auditiva/fisiología , Corteza Cerebral , Lenguaje , Vocalización Animal , Estimulación Acústica , Animales , Evolución Biológica , Corteza Cerebral/anatomía & histología , Corteza Cerebral/fisiología , Femenino , Humanos , Macaca , Imagen por Resonancia Magnética , Masculino , Tomografía de Emisión de Positrones , Distribución Aleatoria , Especificidad de la EspecieRESUMEN
Categorical perception is a fundamental cognitive function enabling animals to flexibly assign sounds into behaviorally relevant categories. This study investigates the nature of acoustic category representations, their emergence in an ascending series of ferret auditory and frontal cortical fields, and the dynamics of this representation during passive listening to task-relevant stimuli and during active retrieval from memory while engaging in learned categorization tasks. Ferrets were trained on two auditory Go-NoGo categorization tasks to discriminate two non-compact sound categories (composed of tones or amplitude-modulated noise). Neuronal responses became progressively more categorical in higher cortical fields, especially during task performance. The dynamics of the categorical responses exhibited a cascading top-down modulation pattern that began earliest in the frontal cortex and subsequently flowed downstream to the secondary auditory cortex, followed by the primary auditory cortex. In a subpopulation of neurons, categorical responses persisted even during the passive listening condition, demonstrating memory for task categories and their enhanced categorical boundaries.
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Corteza Auditiva/fisiología , Percepción Auditiva/fisiología , Lóbulo Frontal/fisiología , Sonido , Estimulación Acústica , Animales , Conducta Animal , Femenino , Hurones , Aprendizaje , Monitoreo FisiológicoRESUMEN
Language has been considered by many to be uniquely human. Numerous theories for how it evolved have been proposed but rarely tested. The articles in this theme issue consider the extent to which aspects of language, such as vocal learning, phonology, syntax, semantics, intentionality, cognition and neurobiological adaptations, are shared with other animals. By adopting a comparative approach, insights into the mechanisms and origins of human language can be gained. While points of agreement exist among the authors, conflicting viewpoints are expressed on several issues, such as the presence of proto-syntax in animal communication, the neural basis of the Merge operation, and the neurogenetic changes necessary for vocal learning. Future comparative research in animal communication has the potential to teach us even more about the evolution, neurobiology and cognitive basis of human language. This article is part of the theme issue 'What can animal communication teach us about human language?'
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Comunicación Animal , Comunicación , Lenguaje , Animales , Evolución Biológica , Cognición/fisiología , Humanos , Aprendizaje/fisiología , Lingüística , Neurobiología , Semántica , Habla , Vocalización AnimalRESUMEN
Recent studies of the neurobiology of the dorsal frontal cortex (FC) of the ferret have illuminated its key role in the attention network, top-down cognitive control of sensory processing, and goal directed behavior. To elucidate the neuroanatomical regions of the dorsal FC, and delineate the boundary between premotor cortex (PMC) and dorsal prefrontal cortex (dPFC), we placed retrograde tracers in adult ferret dorsal FC anterior to primary motor cortex and analyzed thalamo-cortical connectivity. Cyto- and myeloarchitectural differences across dorsal FC and the distinctive projection patterns from thalamic nuclei, especially from the subnuclei of the medial dorsal (MD) nucleus and the ventral thalamic nuclear group, make it possible to clearly differentiate three separate dorsal FC fields anterior to primary motor cortex: polar dPFC (dPFCpol), dPFC, and PMC. Based on the thalamic connectivity, there is a striking similarity of the ferret's dorsal FC fields with other species. This possible homology opens up new questions for future comparative neuroanatomical and functional studies.
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Corteza Motora/citología , Neuronas/citología , Corteza Prefrontal/citología , Núcleos Talámicos/citología , Animales , Femenino , Hurones , Masculino , Vías Nerviosas/citología , Técnicas de Trazados de Vías NeuroanatómicasRESUMEN
Population responses of cortical neurons encode considerable details about sensory stimuli, and the encoded information is likely to change with stimulus context and behavioral conditions. The details of encoding are difficult to discern across large sets of single neuron data because of the complexity of naturally occurring stimulus features and cortical receptive fields. To overcome this problem, we used the method of stimulus reconstruction to study how complex sounds are encoded in primary auditory cortex (AI). This method uses a linear spectro-temporal model to map neural population responses to an estimate of the stimulus spectrogram, thereby enabling a direct comparison between the original stimulus and its reconstruction. By assessing the fidelity of such reconstructions from responses to modulated noise stimuli, we estimated the range over which AI neurons can faithfully encode spectro-temporal features. For stimuli containing statistical regularities (typical of those found in complex natural sounds), we found that knowledge of these regularities substantially improves reconstruction accuracy over reconstructions that do not take advantage of this prior knowledge. Finally, contrasting stimulus reconstructions under different behavioral states showed a novel view of the rapid changes in spectro-temporal response properties induced by attentional and motivational state.
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Corteza Auditiva/citología , Mapeo Encefálico , Modelos Neurológicos , Plasticidad Neuronal/fisiología , Neuronas/fisiología , Estimulación Acústica/métodos , Animales , Simulación por Computador , Potenciales Evocados Auditivos/fisiología , Femenino , HuronesRESUMEN
Some fifty years after the first physiological studies of auditory attention, the field is now ripening, with exciting recent insights into the psychophysics, psychology, and neural basis of auditory attention. Current research seeks to unravel the complex interactions of pre-attentive and attentive processing of the acoustic scene, the role of auditory attention in mediating receptive-field plasticity in both auditory spatial and auditory feature processing, the contrasts and parallels between auditory and visual attention pathways and mechanisms, the interplay of bottom-up and top-down attentional mechanisms, the influential role of attention, goals, and expectations in shaping auditory processing, and the orchestration of diverse attentional effects at multiple levels from the cochlea to the cortex.
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Atención/fisiología , Vías Auditivas/fisiología , Percepción Auditiva/fisiología , Sonido , Percepción Espacial/fisiología , Animales , Humanos , Plasticidad Neuronal/fisiologíaRESUMEN
In higher sensory cortices, there is a gradual transformation from sensation to perception and action. In the auditory system, this transformation is revealed by responses in the rostral ventral posterior auditory field (VPr), a tertiary area in the ferret auditory cortex, which shows long-term learning in trained compared to naïve animals, arising from selectively enhanced responses to behaviorally relevant target stimuli. This enhanced representation is further amplified during active performance of spectral or temporal auditory discrimination tasks. VPr also shows sustained short-term memory activity after target stimulus offset, correlated with task response timing and action. These task-related changes in auditory filter properties enable VPr neurons to quickly and nimbly switch between different responses to the same acoustic stimuli, reflecting either spectrotemporal properties, timing, or behavioral meaning of the sound. Furthermore, they demonstrate an interaction between the dynamics of short-term attention and long-term learning, as incoming sound is selectively attended, recognized, and translated into action.
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Corteza Auditiva/fisiología , Percepción Auditiva/fisiología , Discriminación en Psicología/fisiología , Neuronas/fisiología , Estimulación Acústica , Adaptación Fisiológica , Animales , Conducta Animal , Conducta de Elección , Femenino , HuronesRESUMEN
Previous studies have shown that the auditory cortex can enhance the perception of behaviorally important sounds in the presence of background noise, but the mechanisms by which it does this are not yet elucidated. Rapid plasticity of spectrotemporal receptive fields (STRFs) in the primary (A1) cortical neurons is observed during behavioral tasks that require discrimination of particular sounds. This rapid task-related change is believed to be one of the processing strategies utilized by the auditory cortex to selectively attend to one stream of sound in the presence of mixed sounds. However, the mechanism by which the brain evokes this rapid plasticity in the auditory cortex remains unclear. This paper uses a neural network model to investigate how synaptic transmission within the cortical neuron network can change the receptive fields of individual neurons. A sound signal was used as input to a model of the cochlea and auditory periphery, which activated or inhibited integrate-and-fire neuron models to represent networks in the primary auditory cortex. Each neuron in the network was tuned to a different frequency. All neurons were interconnected with excitatory or inhibitory synapses of varying strengths. Action potentials in one of the model neurons were used to calculate the receptive field using reverse correlation. The results were directly compared to previously recorded electrophysiological data from ferrets performing behavioral tasks that require discrimination of particular sounds. The neural network model could reproduce complex STRFs observed experimentally through optimizing the synaptic weights in the model. The model predicts that altering synaptic drive between cortical neurons and/or bottom-up synaptic drive from the cochlear model to the cortical neurons can account for rapid task-related changes observed experimentally in A1 neurons. By identifying changes in the synaptic drive during behavioral tasks, the model provides insights into the neural mechanisms utilized by the auditory cortex to enhance the perception of behaviorally salient sounds.
RESUMEN
To form a reliable, consistent, and accurate representation of the acoustic scene, a reasonable conjecture is that cortical neurons maintain stable receptive fields after an early period of developmental plasticity. However, recent studies suggest that cortical neurons can be modified throughout adulthood and may change their response properties quite rapidly to reflect changing behavioral salience of certain sensory features. Because claims of adaptive receptive field plasticity could be confounded by intrinsic, labile properties of receptive fields themselves, we sought to gauge spontaneous changes in the responses of auditory cortical neurons. In the present study, we examined changes in a series of spectrotemporal receptive fields (STRFs) gathered from single neurons in successive recordings obtained over time scales of 30-120 min in primary auditory cortex (A1) in the quiescent, awake ferret. We used a global analysis of STRF shape based on a large database of A1 receptive fields. By clustering this STRF space in a data-driven manner, STRF sequences could be classified as stable or labile. We found that >73% of A1 neurons exhibited stable receptive field attributes over these time scales. In addition, we found that the extent of intrinsic variation in STRFs during the quiescent state was insignificant compared with behaviorally induced STRF changes observed during performance of spectral auditory tasks. Our results confirm that task-related changes induced by attentional focus on specific acoustic features were indeed confined to behaviorally salient acoustic cues and could be convincingly attributed to learning-induced plasticity when compared with "spontaneous" receptive field variability.