Spectral-Temporal Receptive Fields of Nonlinear Auditory Neurons Obtained Using Natural Sounds

We estimated the spectrotemporal receptive fields of neurons in the songbird auditory thalamus, nucleus ovoidalis, and compared the neural representation of complex sounds in the auditory thalamus to those found in the upstream auditory midbrain nucleus, mesencephalicus lateralis dorsalis (MLd), and the downstream auditory pallial region, field L. Our data refute the idea that the primary sensory thalamus acts as a simple, relay nucleus: we find that the auditory thalamic receptive fields obtained in response to song are more complex than the ones found in the midbrain. Moreover, we find that linear tuning diversity and complexity in ovoidalis (Ov) are closer to those found in field L than in MLd. We also find prevalent tuning to intermediate spectral and temporal modulations, a feature that is unique to Ov. Thus even a feed-forward model of the sensory processing chain, where neural responses in the sensory thalamus reveals intermediate response properties between those in the sensory periphery and those in the primary sensory cortex, is inadequate in describing the tuning found in Ov. Based on these results, we believe that the auditory thalamic circuitry plays an important role in generating novel complex representations for specific features found in natural sounds.

Download Full-text

Delayed Inhibition in Cortical Receptive Fields and the Discrimination of Complex Stimuli

Journal of Neurophysiology ◽

10.1152/jn.00144.2005 ◽

2005 ◽

Vol 94 (4) ◽

pp. 2970-2975 ◽

Cited By ~ 18

Author(s):

Rajiv Narayan ◽

Ayla Ergün ◽

Kamal Sen

Keyword(s):

Auditory Cortex ◽

Temporal Structure ◽

Receptive Fields ◽

Primary Auditory Cortex ◽

Natural Sounds ◽

Functional Roles ◽

Complex Stimuli ◽

Animal Vocalizations ◽

Field L ◽

Cortical Receptive Fields

Although auditory cortex is thought to play an important role in processing complex natural sounds such as speech and animal vocalizations, the specific functional roles of cortical receptive fields (RFs) remain unclear. Here, we study the relationship between a behaviorally important function: the discrimination of natural sounds and the structure of cortical RFs. We examine this problem in the model system of songbirds, using a computational approach. First, we constructed model neurons based on the spectral temporal RF (STRF), a widely used description of auditory cortical RFs. We focused on delayed inhibitory STRFs, a class of STRFs experimentally observed in primary auditory cortex (ACx) and its analog in songbirds (field L), which consist of an excitatory subregion and a delayed inhibitory subregion cotuned to a characteristic frequency. We quantified the discrimination of birdsongs by model neurons, examining both the dynamics and temporal resolution of discrimination, using a recently proposed spike distance metric (SDM). We found that single model neurons with delayed inhibitory STRFs can discriminate accurately between songs. Discrimination improves dramatically when the temporal structure of the neural response at fine timescales is considered. When we compared discrimination by model neurons with and without the inhibitory subregion, we found that the presence of the inhibitory subregion can improve discrimination. Finally, we modeled a cortical microcircuit with delayed synaptic inhibition, a candidate mechanism underlying delayed inhibitory STRFs, and showed that blocking inhibition in this model circuit degrades discrimination.

Download Full-text

Representations of Conspecific Song by Starling Secondary Forebrain Auditory Neurons: Toward a Hierarchical Framework

Journal of Neurophysiology ◽

10.1152/jn.00464.2009 ◽

2010 ◽

Vol 103 (3) ◽

pp. 1195-1208 ◽

Cited By ~ 25

Author(s):

C. Daniel Meliza ◽

Zhiyi Chi ◽

Daniel Margoliash

Keyword(s):

Predictive Power ◽

Functional Organization ◽

Receptive Fields ◽

Spike Timing ◽

Auditory Neurons ◽

Linear Summation ◽

European Starlings ◽

Spike Timing Precision ◽

Spectrotemporal Receptive Field ◽

Spike Waveforms

The functional organization giving rise to stimulus selectivity in higher-order auditory neurons remains under active study. We explored the selectivity for motifs, spectrotemporally distinct perceptual units in starling song, recording the responses of 96 caudomedial mesopallium (CMM) neurons in European starlings ( Sturnus vulgaris) under awake-restrained and urethane-anesthetized conditions. A subset of neurons was highly selective between motifs. Selectivity was correlated with low spontaneous firing rates and high spike timing precision, and all but one of the selective neurons had similar spike waveforms. Neurons were further tested with stimuli in which the notes comprising the motifs were manipulated. Responses to most of the isolated notes were similar in amplitude, duration, and temporal pattern to the responses elicited by those notes in the context of the motif. For these neurons, we could accurately predict the responses to motifs from the sum of the responses to notes. Some notes were suppressed by the motif context, such that removing other notes from motifs unmasked additional excitation. Models of linear summation of note responses consistently outperformed spectrotemporal receptive field models in predicting responses to song stimuli. Tests with randomized sequences of notes confirmed the predictive power of these models. Whole notes gave better predictions than did note fragments. Thus in CMM, auditory objects (motifs) can be represented by a linear combination of excitation and suppression elicited by the note components of the object. We hypothesize that the receptive fields arise from selective convergence by inputs responding to specific spectrotemporal features of starling notes.

Download Full-text

Linearity of Cortical Receptive Fields Measured with Natural Sounds

Journal of Neuroscience ◽

10.1523/jneurosci.4445-03.2004 ◽

2004 ◽

Vol 24 (5) ◽

pp. 1089-1100 ◽

Cited By ~ 169

Author(s):

C. K. Machens

Keyword(s):

Receptive Fields ◽

Natural Sounds ◽

Cortical Receptive Fields

Download Full-text

Central auditory neurons have composite receptive fields

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1506903113 ◽

2016 ◽

Vol 113 (5) ◽

pp. 1441-1446 ◽

Cited By ~ 33

Author(s):

Andrei S. Kozlov ◽

Timothy Q. Gentner

Keyword(s):

Neural Circuits ◽

Receptive Fields ◽

Learning Rule ◽

Auditory Neurons ◽

Olfactory Neurons ◽

Unsupervised Neural Network ◽

Divisive Normalization ◽

Vocal Signals ◽

Central Auditory Neurons ◽

High Level

High-level neurons processing complex, behaviorally relevant signals are sensitive to conjunctions of features. Characterizing the receptive fields of such neurons is difficult with standard statistical tools, however, and the principles governing their organization remain poorly understood. Here, we demonstrate multiple distinct receptive-field features in individual high-level auditory neurons in a songbird, European starling, in response to natural vocal signals (songs). We then show that receptive fields with similar characteristics can be reproduced by an unsupervised neural network trained to represent starling songs with a single learning rule that enforces sparseness and divisive normalization. We conclude that central auditory neurons have composite receptive fields that can arise through a combination of sparseness and normalization in neural circuits. Our results, along with descriptions of random, discontinuous receptive fields in the central olfactory neurons in mammals and insects, suggest general principles of neural computation across sensory systems and animal classes.

Download Full-text