Improved stimulus representation by short interspike intervals in primary auditory cortex

We analyzed the receptive field information conveyed by interspike intervals (ISIs) in the auditory cortex. In the visual system, different ISIs may both code for different visual features and convey differing amounts of stimulus information. To determine their potential role in auditory signal processing, we obtained extracellular recordings in the primary auditory cortex (AI) of the cat while presenting a dynamic moving ripple stimulus and then used the responses to construct spectrotemporal receptive fields (STRFs). For each neuron, we constructed three STRFs, one for short-ISI events (ISI < 15 ms); one for isolated, long-ISI events (ISI > 15 ms); and one including all events. To characterize stimulus encoding, we calculated the feature selectivity and event information for each of the STRFs. Short-ISI spikes were more feature selective and conveyed information more efficiently. The different ISI regimens of AI neurons did not represent different stimulus features, but short-ISI spike events did contribute over-proportionately to the full spike train STRF information. Thus short-ISIs constitute a robust representation of auditory features, and they are particularly effective at driving postsynaptic activity. This suggests that short-ISI events are especially suited to provide noise immunity and high-fidelity information transmission in AI.

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Active listening: Task-dependent plasticity of spectrotemporal receptive fields in primary auditory cortex

Hearing Research ◽

10.1016/j.heares.2005.01.015 ◽

2005 ◽

Vol 206 (1-2) ◽

pp. 159-176 ◽

Cited By ~ 116

Author(s):

Jonathan Fritz ◽

Mounya Elhilali ◽

Shihab Shamma

Keyword(s):

Auditory Cortex ◽

Receptive Fields ◽

Primary Auditory Cortex ◽

Active Listening ◽

Dependent Plasticity ◽

Spectrotemporal Receptive Fields ◽

Listening Task

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Spectrotemporal Structure of Receptive Fields in Areas AI and AAF of Mouse Auditory Cortex

Journal of Neurophysiology ◽

10.1152/jn.00751.2002 ◽

2003 ◽

Vol 90 (4) ◽

pp. 2660-2675 ◽

Cited By ~ 156

Author(s):

Jennifer F. Linden ◽

Robert C. Liu ◽

Maneesh Sahani ◽

Christoph E. Schreiner ◽

Michael M. Merzenich

Keyword(s):

Receptive Field ◽

Auditory Cortex ◽

Receptive Fields ◽

Primary Auditory Cortex ◽

Dynamic Stimuli ◽

Tuning Curves ◽

Response Characteristics ◽

Spectrotemporal Receptive Fields ◽

Auditory Field ◽

Tonal Stimuli

The mouse is a promising model system for auditory cortex research because of the powerful genetic tools available for manipulating its neural circuitry. Previous studies have identified two tonotopic auditory areas in the mouse—primary auditory cortex (AI) and anterior auditory field (AAF)— but auditory receptive fields in these areas have not yet been described. To establish a foundation for investigating auditory cortical circuitry and plasticity in the mouse, we characterized receptive-field structure in AI and AAF of anesthetized mice using spectrally complex and temporally dynamic stimuli as well as simple tonal stimuli. Spectrotemporal receptive fields (STRFs) were derived from extracellularly recorded responses to complex stimuli, and frequency-intensity tuning curves were constructed from responses to simple tonal stimuli. Both analyses revealed temporal differences between AI and AAF responses: peak latencies and receptive-field durations for STRFs and first-spike latencies for responses to tone bursts were significantly longer in AI than in AAF. Spectral properties of AI and AAF receptive fields were more similar, although STRF bandwidths were slightly broader in AI than in AAF. Finally, in both AI and AAF, a substantial minority of STRFs were spectrotemporally inseparable. The spectrotemporal interaction typically appeared in the form of clearly disjoint excitatory and inhibitory subfields or an obvious spectrotemporal slant in the STRF. These data provide the first detailed description of auditory receptive fields in the mouse and suggest that although neurons in areas AI and AAF share many response characteristics, area AAF may be specialized for faster temporal processing.

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A complex feature-based representation of vocalizations emerges in the superficial layers of primary auditory cortex

10.1101/2021.04.11.439331 ◽

2021 ◽

Author(s):

Pilar Montes-Lourido ◽

Manaswini Kar ◽

Stephen V David ◽

Srivatsun Sadagopan

Keyword(s):

Auditory Cortex ◽

Auditory Processing ◽

Receptive Fields ◽

Primary Auditory Cortex ◽

Neural Representation ◽

Specific Information ◽

Intermediate Step ◽

Stimulus Information ◽

Feature Selectivity ◽

Feature Based

Early in auditory processing, neural responses faithfully reflect acoustic input. At higher stages of auditory processing, however, neurons become selective for particular call types, eventually leading to specialized regions of cortex that preferentially process calls at the highest auditory processing stages. We previously proposed that an intermediate step in how non-selective responses are transformed into call-selective responses is the detection of informative call features. But how neural selectivity for informative call features emerges from non-selective inputs, whether feature selectivity gradually emerges over the processing hierarchy, and how stimulus information is represented in non-selective and feature-selective populations remain open questions. In this study, using unanesthetized guinea pigs, a highly vocal and social rodent, as an animal model, we characterized the neural representation of calls in three auditory processing stages: the thalamus (vMGB), and thalamorecipient (L4) and superficial layers (L2/3) of primary auditory cortex (A1). We found that neurons in vMGB and A1 L4 did not exhibit call-selective responses and responded throughout the call durations. However, A1 L2/3 neurons showed high call-selectivity with about a third of neurons responding to only one or two call types. These A1 L2/3 neurons only responded to restricted portions of calls suggesting that they were highly selective for call features. Receptive fields of these A1 L2/3 neurons showed complex spectrotemporal structures that could underlie their high call feature selectivity. Information theoretic analysis revealed that in A1 L4 stimulus information was distributed over the population and was spread out over the call durations. In contrast, in A1 L2/3, individual neurons showed brief bursts of high stimulus-specific information, and conveyed high levels of information per spike. These data demonstrate that a transformation in the neural representation of calls occurs between A1 L4 and A1 L2/3, leading to the emergence of a feature-based representation of calls in A1 L2/3. Our data thus suggest that observed cortical specializations for call processing emerge in A1, and set the stage for further mechanistic studies.

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Frequency-Modulation Encoding in the Primary Auditory Cortex of the Awake Owl Monkey

Journal of Neurophysiology ◽

10.1152/jn.00394.2007 ◽

2007 ◽

Vol 98 (4) ◽

pp. 2182-2195 ◽

Cited By ~ 40

Author(s):

Craig A. Atencio ◽

David T. Blake ◽

Fabrizio Strata ◽

Steven W. Cheung ◽

Michael M. Merzenich ◽

...

Keyword(s):

Auditory Cortex ◽

World Monkey ◽

Receptive Fields ◽

Primary Auditory Cortex ◽

Direction Selectivity ◽

Neural Responses ◽

Population Distributions ◽

Spectrotemporal Receptive Fields ◽

Owl Monkey ◽

Highly Correlated

Many communication sounds, such as New World monkey twitter calls, contain frequency-modulated (FM) sweeps. To determine how this prominent vocalization element is represented in the auditory cortex we examined neural responses to logarithmic FM sweep stimuli in the primary auditory cortex (AI) of two awake owl monkeys. Using an implanted array of microelectrodes we quantitatively characterized neuronal responses to FM sweeps and to random tone-pip stimuli. Tone-pip responses were used to construct spectrotemporal receptive fields (STRFs). Classification of FM sweep responses revealed few neurons with high direction and speed selectivity. Most neurons responded to sweeps in both directions and over a broad range of sweep speeds. Characteristic frequency estimates from FM responses were highly correlated with estimates from STRFs, although spectral receptive field bandwidth was consistently underestimated by FM stimuli. Predictions of FM direction selectivity and best speed from STRFs were significantly correlated with observed FM responses, although some systematic discrepancies existed. Last, the population distributions of FM responses in the awake owl monkey were similar to, although of longer temporal duration than, those in the anesthetized squirrel monkeys.

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Laminar Diversity of Dynamic Sound Processing in Cat Primary Auditory Cortex

Journal of Neurophysiology ◽

10.1152/jn.00624.2009 ◽

2010 ◽

Vol 103 (1) ◽

pp. 192-205 ◽

Cited By ~ 40

Author(s):

Craig A. Atencio ◽

Christoph E. Schreiner

Keyword(s):

Auditory Cortex ◽

Transfer Functions ◽

Receptive Fields ◽

Primary Auditory Cortex ◽

Functional Characteristic ◽

Modulation Transfer ◽

Spectral Modulation ◽

Spectrotemporal Receptive Fields ◽

Low Pass ◽

Acoustic Modulation

For primary auditory cortex (AI) laminae, there is little evidence of functional specificity despite clearly expressed cellular and connectional differences. Natural sounds are dominated by dynamic temporal and spectral modulations and we used these properties to evaluate local functional differences or constancies across laminae. To examine the layer-specific processing of acoustic modulation information, we simultaneously recorded from multiple AI laminae in the anesthetized cat. Neurons were challenged with dynamic moving ripple stimuli and we subsequently computed spectrotemporal receptive fields (STRFs). From the STRFs, temporal and spectral modulation transfer functions (tMTFs, sMTFs) were calculated and compared across layers. Temporal and spectral modulation properties often differed between layers. On average, layer II/III and VI neurons responded to lower temporal modulations than those in layer IV. tMTFs were mainly band-pass in granular layer IV and became more low-pass in infragranular layers. Compared with layer IV, spectral MTFs were broader and their upper cutoff frequencies higher in layers V and VI. In individual penetrations, temporal modulation preference was similar across layers for roughly 70% of the penetrations, suggesting a common, columnar functional characteristic. By contrast, only about 30% of penetrations showed consistent spectral modulation preferences across layers, indicative of functional laminar diversity or specialization. Since local laminar differences in stimulus preference do not always parallel the main flow of information in the columnar cortical microcircuit, this indicates the influence of additional horizontal or thalamocortical inputs. AI layers that express differing modulation properties may serve distinct roles in the extraction of dynamic sound information, with the differing information specific to the targeted stations of each layer.

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