Spectrotemporal Organization of Excitatory and Inhibitory Receptive Fields of Cat Posterior Auditory Field Neurons

2001 ◽  
Vol 86 (1) ◽  
pp. 475-491 ◽  
Author(s):  
William C. Loftus ◽  
Mitchell L. Sutter
Keyword(s):  
Response Times ◽  
Frequency Tuning ◽  
Population Analysis ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Stimulus Onset ◽  
Spike Response ◽  
Threshold Response ◽  
Spectrotemporal Receptive Fields ◽  
Auditory Field

The excitatory and inhibitory frequency/intensity response areas (FRAs) and spectrotemporal receptive fields (STRFs) of posterior auditory cortical field (PAF) single neurons were investigated in barbiturate anesthetized cats. PAF neurons' pure-tone excitatory FRAs (eFRAs) exhibited a diversity of shapes, including some with very broad frequency tuning and some with multiple distinct excitatory frequency ranges (i.e., multipeaked eFRAs). Excitatory FRAs were analyzed after selectively excluding spikes on the basis of spike response times relative to stimulus onset. This analysis indicated that spikes with shorter response times were confined to narrow regions of the eFRAs, while spikes with longer response times were more broadly distributed over the eFRA. First-spike latencies in higher threshold response peaks of multipeaked eFRAs were ∼10 ms longer, on average, than latencies in lower threshold response peaks. STRFs were constructed to examine the dynamic frequency tuning of neurons. More than half of the neurons (51%) had STRFs with “sloped” response maxima, indicating that the excitatory frequency range shifted with time. A population analysis demonstrated that the median first-spike latency varied systematically as a function of frequency with a median slope of ∼12 ms per octave. Inhibitory frequency response areas were determined by simultaneous two-tone stimulation. As in primary auditory cortex (A1), a diversity of inhibitory band structures was observed. The largest class of neurons (25%) had an inhibitory band flanking each eFRA edge, i.e., one lower and one upper inhibitory band in a “center-surround” organization. However, in comparison to a previous report of inhibitory structure in A1 neurons, PAF exhibited a higher incidence of neurons with more complex inhibitory band structure (for example, >2 inhibitory bands). As was the case with eFRAs, spikes with longer response times contributed to the complexity of inhibitory FRAs. These data indicate that PAF neurons integrate temporally varying excitatory and inhibitory inputs from a broad spectral extent and, compared with A1, may be suited to analyzing acoustic signals of greater spectrotemporal complexity than was previously thought.

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

2003 ◽  
Vol 90 (4) ◽  
pp. 2660-2675 ◽  
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.

scholarly journals Reorganization in processing of spectral and temporal input in the rat posterior auditory field induced by environmental enrichment

2012 ◽  
Vol 107 (5) ◽  
pp. 1457-1475 ◽  
Author(s):  
Vikram Jakkamsetti ◽  
Kevin Q. Chang ◽  
Michael P. Kilgard
Keyword(s):  
Environmental Enrichment ◽  
Sensory Input ◽  
Response Times ◽  
Neuronal Response ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Response Strength ◽  
Sensory Cortex ◽  
Primary Sensory Cortex ◽  
Auditory Field

Environmental enrichment induces powerful changes in the adult cerebral cortex. Studies in primary sensory cortex have observed that environmental enrichment modulates neuronal response strength, selectivity, speed of response, and synchronization to rapid sensory input. Other reports suggest that nonprimary sensory fields are more plastic than primary sensory cortex. The consequences of environmental enrichment on information processing in nonprimary sensory cortex have yet to be studied. Here we examine physiological effects of enrichment in the posterior auditory field (PAF), a field distinguished from primary auditory cortex (A1) by wider receptive fields, slower response times, and a greater preference for slowly modulated sounds. Environmental enrichment induced a significant increase in spectral and temporal selectivity in PAF. PAF neurons exhibited narrower receptive fields and responded significantly faster and for a briefer period to sounds after enrichment. Enrichment increased time-locking to rapidly successive sensory input in PAF neurons. Compared with previous enrichment studies in A1, we observe a greater magnitude of reorganization in PAF after environmental enrichment. Along with other reports observing greater reorganization in nonprimary sensory cortex, our results in PAF suggest that nonprimary fields might have a greater capacity for reorganization compared with primary fields.

scholarly journals Facilitatory and Inhibitory Frequency Tuning of Combination-Sensitive Neurons in the Primary Auditory Cortex of Mustached Bats

1999 ◽  
Vol 82 (5) ◽  
pp. 2327-2345 ◽  
Author(s):  
Jagmeet S. Kanwal ◽  
Douglas C. Fitzpatrick ◽  
Nobuo Suga
Keyword(s):  
Auditory Cortex ◽  
Frequency Tuning ◽  
Temporal Structure ◽  
Primary Auditory Cortex ◽  
Frequency Discrimination ◽  
Inhibitory Response ◽  
Center Frequency ◽  
Constant Frequency ◽  
Single Tone ◽  
Threshold Response

Mustached bats, Pteronotus parnellii parnellii,emit echolocation pulses that consist of four harmonics with a fundamental consisting of a constant frequency (CF1-4) component followed by a short, frequency-modulated (FM1-4) component. During flight, the pulse fundamental frequency is systematically lowered by an amount proportional to the velocity of the bat relative to the background so that the Doppler-shifted echo CF2 is maintained within a narrowband centered at ∼61 kHz. In the primary auditory cortex, there is an expanded representation of 60.6- to 63.0-kHz frequencies in the “Doppler-shifted CF processing” (DSCF) area where neurons show sharp, level-tolerant frequency tuning. More than 80% of DSCF neurons are facilitated by specific frequency combinations of ∼25 kHz (BFlow) and ∼61 kHz (BFhigh). To examine the role of these neurons for fine frequency discrimination during echolocation, we measured the basic response parameters for facilitation to synthesized echolocation signals varied in frequency, intensity, and in their temporal structure. Excitatory response areas were determined by presenting single CF tones, facilitative curves were obtained by presenting paired CF tones. All neurons showing facilitation exhibit at least two facilitative response areas, one of broad spectral tuning to frequencies centered at BFlowcorresponding to a frequency in the lower half of the echolocation pulse FM1 sweep and another of sharp tuning to frequencies centered at BFhigh corresponding to the CF2 in the echo. Facilitative response areas for BFhigh are broadened by ∼0.38 kHz at both the best amplitude and 50 dB above threshold response and show lower thresholds compared with the single-tone excitatory BFhigh response areas. An increase in the sensitivity of DSCF neurons would lead to target detection from farther away and/or for smaller targets than previously estimated on the basis of single-tone responses to BFhigh. About 15% of DSCF neurons show oblique excitatory and facilitatory response areas at BFhigh so that the center frequency of the frequency-response function at any amplitude decreases with increasing stimulus amplitudes. DSCF neurons also have inhibitory response areas that either skirt or overlap both the excitatory and facilitatory response areas for BFhigh and sometimes for BFlow. Inhibition by a broad range of frequencies contributes to the observed sharpness of frequency tuning in these neurons. Recordings from orthogonal penetrations show that the best frequencies for facilitation as well as excitation do not change within a cortical column. There does not appear to be any systematic representation of facilitation ratios across the cortical surface of the DSCF area.

scholarly journals Dissociable influences of primary auditory cortex and the posterior auditory field on neuronal responses in the dorsal zone of auditory cortex

2015 ◽  
Vol 113 (2) ◽  
pp. 475-486
Author(s):  
Melanie A. Kok ◽  
Daniel Stolzberg ◽  
Trecia A. Brown ◽  
Stephen G. Lomber
Keyword(s):  
Auditory Cortex ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Population Level ◽  
Noise Burst ◽  
Hierarchical Organization ◽  
Neuronal Responses ◽  
Tone Frequency ◽  
Hierarchical Processing ◽  
Auditory Field

Current models of hierarchical processing in auditory cortex have been based principally on anatomical connectivity while functional interactions between individual regions have remained largely unexplored. Previous cortical deactivation studies in the cat have addressed functional reciprocal connectivity between primary auditory cortex (A1) and other hierarchically lower level fields. The present study sought to assess the functional contribution of inputs along multiple stages of the current hierarchical model to a higher order area, the dorsal zone (DZ) of auditory cortex, in the anaesthetized cat. Cryoloops were placed over A1 and posterior auditory field (PAF). Multiunit neuronal responses to noise burst and tonal stimuli were recorded in DZ during cortical deactivation of each field individually and in concert. Deactivation of A1 suppressed peak neuronal responses in DZ regardless of stimulus and resulted in increased minimum thresholds and reduced absolute bandwidths for tone frequency receptive fields in DZ. PAF deactivation had less robust effects on DZ firing rates and receptive fields compared with A1 deactivation, and combined A1/PAF cooling was largely driven by the effects of A1 deactivation at the population level. These results provide physiological support for the current anatomically based model of both serial and parallel processing schemes in auditory cortical hierarchical organization.

scholarly journals Complexity of frequency receptive fields predicts tonotopic variability across species

2019 ◽  
Author(s):  
Quentin Gaucher ◽  
Mariangela Panniello ◽  
Aleksandar Z Ivanov ◽  
Johannes C Dahmen ◽  
Andrew J King ◽  
...  
Keyword(s):  
Large Scale ◽  
Frequency Tuning ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Single Frequency ◽  
Complex Frequency ◽  
Two Photon ◽  
Local Variance ◽  
Sensory Features ◽  
Local Variability

AbstractPrimary cortical areas contain maps of sensory features, including sound frequency in primary auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these large-scale maps, while uncovering an unexpected local variability in the stimulus preferences of individual neurons in A1 and other primary regions. Here we show that fractured tonotopy is not unique to rodents. Using two-photon imaging, we found that local variance in frequency preferences is equivalent in ferrets and mice. Much of this heterogeneity was due to neurons with complex frequency tuning, which are less spatially organized than those tuned to a single frequency. Finally, we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a bias towards neurons with simple frequency tuning. These results show that local variability in the tonotopic map is not restricted to rodents and help explain inconsistencies in cortical topography across species and recording techniques.

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

2007 ◽  
Vol 98 (4) ◽  
pp. 2182-2195 ◽  
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.

scholarly journals Laminar Diversity of Dynamic Sound Processing in Cat Primary Auditory Cortex

2010 ◽  
Vol 103 (1) ◽  
pp. 192-205 ◽  
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.

scholarly journals Contextual and cross-modality modulation of auditory cortical processing through pulvinar mediated suppression

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Xiao-lin Chou ◽  
Qi Fang ◽  
Linqing Yan ◽  
Wen Zhong ◽  
Bo Peng ◽  
...  
Keyword(s):  
Auditory Processing ◽  
Frequency Tuning ◽  
Signal To Noise Ratio ◽  
Receptive Fields ◽  
Primary Auditory Cortex ◽  
Inhibitory Neurons ◽  
Cortical Processing ◽  
Lateral Posterior ◽  
Sensory Cortices ◽  
Lateral Posterior Nucleus

Lateral posterior nucleus (LP) of thalamus, the rodent homologue of primate pulvinar, projects extensively to sensory cortices. However, its functional role in sensory cortical processing remains largely unclear. Here, bidirectional activity modulations of LP or its projection to the primary auditory cortex (A1) in awake mice reveal that LP improves auditory processing in A1 supragranular-layer neurons by sharpening their receptive fields and frequency tuning, as well as increasing the signal-to-noise ratio (SNR). This is achieved through a subtractive-suppression mechanism, mediated largely by LP-to-A1 axons preferentially innervating specific inhibitory neurons in layer 1 and superficial layers. LP is strongly activated by specific sensory signals relayed from the superior colliculus (SC), contributing to the maintenance and enhancement of A1 processing in the presence of auditory background noise and threatening visual looming stimuli respectively. Thus, a multisensory bottom-up SC-pulvinar-A1 pathway plays a role in contextual and cross-modality modulation of auditory cortical processing.

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