Laminar Diversity of Dynamic Sound Processing in Cat Primary Auditory Cortex

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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Temporal Modulation Transfer Functions in Cat Primary Auditory Cortex: Separating Stimulus Effects From Neural Mechanisms

Journal of Neurophysiology ◽

10.1152/jn.00490.2001 ◽

2002 ◽

Vol 87 (1) ◽

pp. 305-321 ◽

Cited By ~ 72

Author(s):

Jos J. Eggermont

Keyword(s):

Auditory Cortex ◽

Cortical Neurons ◽

Transfer Functions ◽

Frequency Tuning ◽

Primary Auditory Cortex ◽

Modulation Transfer ◽

Temporal Modulation ◽

Pass Filter ◽

Low Pass Filter ◽

Low Pass

We present here a comparison between the local field potentials (LFP) and multiunit (MU) responses, comprising 401 single units, in primary auditory cortex (AI) of 31 cats to periodic click trains, gamma-tone and time-reversed gamma-tone trains, AM noise, AM tones, and frequency-modulated (FM) tones. In a large number of cases, the response to all six stimuli was obtained for the same neurons. We investigate whether cortical neurons are likely to respond to all types of repetitive transients and modulated stimuli and whether a dependence on modulating waveform, or tone or noise carrier, exists. In 97% of the recordings, a temporal modulation transfer function (tMTF) for MU activity was obtained for gamma-tone trains, in 92% for periodic click trains, in 83% for time-reversed gamma-tone trains, in 82% for AM noise, in 71% for FM tones, and only in 53% for AM tones. In 31% of the cases, the units responded to all six stimuli in an envelope-following way. These particular units had significantly larger onset responses to each stimulus compared with all other units. The overall response distribution shows the preference of AI units for stimuli with short rise times such as clicks and gamma tones. It also shows a clear asymmetry in the ability to respond to AM noise and AM tones and points to a strong effect of the frequency content of the carrier on the subcortical processing of AM stimuli. Yet all temporal response properties were independent of characteristic frequency and frequency-tuning curve bandwidth. We show that the observed differences in the tMTFs for different stimuli are to a large extent produced by the different degree of phase locking of the neuronal firings to the envelope of the first stimulus in the train or first modulation period. A normalization procedure, based on these synchronization differences, unified the tMTFs for all stimuli except clicks and allowed the identification of a largely stimulus-invariant, low-pass temporal filter function that most likely reflects the properties of synaptic depression and facilitation. For nonclick stimuli, the low-pass filter has a cutoff frequency of ∼10 Hz and a slope of ∼6 dB/octave. For nonclick stimuli, there was a systematic difference between the vector strength for LFPs and MU activity that can likely be attributed to postactivation suppression mechanisms.

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Wiener-Volterra Characterization of Neurons in Primary Auditory Cortex Using Poisson-Distributed Impulse Train Inputs

Journal of Neurophysiology ◽

10.1152/jn.91242.2008 ◽

2009 ◽

Vol 101 (6) ◽

pp. 3031-3041 ◽

Cited By ~ 9

Author(s):

Martin Pienkowski ◽

Greg Shaw ◽

Jos J. Eggermont

Keyword(s):

Auditory Cortex ◽

Impulse Response ◽

Transfer Functions ◽

Modulation Frequency ◽

Primary Auditory Cortex ◽

Second Order ◽

Modulation Transfer ◽

Low Pass ◽

Time Courses ◽

Impulse Train

An extension of the Wiener-Volterra theory to a Poisson-distributed impulse train input was used to characterize the temporal response properties of neurons in primary auditory cortex (AI) of the ketamine-anesthetized cat. Both first- and second-order “Poisson-Wiener” (PW) models were tested on their predictions of temporal modulation transfer functions (tMTFs), which were derived from extracellular spike responses to periodic click trains with click repetition rates of 2–64 Hz. Second-order (i.e., nonlinear) PW fits to the measured tMTFs could be described as very good in a majority of cases (e.g., predictability ≥80%) and were almost always superior to first-order (i.e., linear) fits. In all sampled neurons, second-order PW kernels showed strong compressive nonlinearities (i.e., a depression of the impulse response) but never expansive nonlinearities (i.e., a facilitation of the impulse response). In neurons with low-pass tMTFs, the depression decayed exponentially with the interstimulus lag, whereas in neurons with band-pass tMTFs, the depression was typically double-peaked, and the second peak occurred at a lag that correlated with the neuron's best modulation frequency. It appears that modulation-tuning in AI arises in part from an interplay of two nonlinear processes with distinct time courses.

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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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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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