Cat Primary Auditory Cortex Research Articles

A comparison of multisensory features of two auditory cortical areas: primary (A1) and higher-order dorsal zone (DZ).

From myriads of ongoing stimuli, the brain creates a fused percept of the environment. This process, which culminates in perceptual binding, is presumed to occur through the operations of multisensory neurons that occur throughout the brain. However, because different brain areas receive different inputs and have different cytoarchitechtonics, it would be expected that local multisensory features would also vary across regions. The present study investigated that hypothesis using multiple single-unit recordings from anesthetized cats in response to controlled, electronically-generated separate and combined auditory, visual, and somatosensory stimulation. These results were used to compare the multisensory features of neurons in cat primary auditory cortex (A1) with those identified in the nearby higher-order auditory region, the Dorsal Zone (DZ). Both regions exhibited the same forms of multisensory neurons, albeit in different proportions. Multisensory neurons exhibiting excitatory or inhibitory properties occurred in similar proportions in both areas. Also, multisensory neurons in both areas expressed similar levels of multisensory integration. Because responses to auditory cues alone were so similar to those that included non-auditory stimuli, it is proposed that this effect represents a mechanism by which multisensory neurons subserve the process of perceptual binding.

Spatial Mechanisms for Segregation of Competing Sounds, and a Breakdown in Spatial Hearing.

We live in complex auditory environments, in which we are confronted with multiple competing sounds, including the cacophony of talkers in busy markets, classrooms, offices, etc. The purpose of this article is to synthesize observations from a series of experiments that focused on how spatial hearing might aid in disentangling interleaved sequences of sounds. The experiments were unified by a non-verbal task, “rhythmic masking release”, which was applied to psychophysical studies in humans and cats and to cortical physiology in anesthetized cats. Human and feline listeners could segregate competing sequences of sounds from sources that were separated by as little as ∼10°. Similarly, single neurons in the cat primary auditory cortex tended to synchronize selectively to sound sequences from one of two competing sources, again with spatial resolution of ∼10°. The spatial resolution of spatial stream segregation varied widely depending on the binaural and monaural acoustical cues that were available in various experimental conditions. This is in contrast to a measure of basic sound-source localization, the minimum audible angle, which showed largely constant acuity across those conditions. The differential utilization of acoustical cues suggests that the central spatial mechanisms for stream segregation differ from those for sound localization. The highest-acuity spatial stream segregation was derived from interaural time and level differences. Brainstem processing of those cues is thought to rely heavily on normal function of a voltage-gated potassium channel, Kv3.3. A family was studied having a dominant negative mutation in the gene for that channel. Affected family members exhibited severe loss of sensitivity for interaural time and level differences, which almost certainly would degrade their ability to segregate competing sounds in real-world auditory scenes.

Spatial Cues Influence Time Estimations in Deaf Individuals.

SummaryRecent studies have reported a strong interaction between spatial and temporal representation when visual experience is missing: blind people use temporal representation of events to represent spatial metrics. Given the superiority of audition on time perception, we hypothesized that when audition is not available complex temporal representations could be impaired, and spatial representation of events could be used to build temporal metrics. To test this hypothesis, deaf and hearing subjects were tested with a visual temporal task where conflicting and not conflicting spatiotemporal information was delivered. As predicted, we observed a strong deficit of deaf participants when only temporal cues were useful and space was uninformative with respect to time. However, the deficit disappeared when coherent spatiotemporal cues were presented and increased for conflicting spatiotemporal stimuli. These results highlight that spatial cues influence time estimations in deaf participants, suggesting that deaf individuals use spatial information to infer temporal environmental coordinates.

Second spatial derivative analysis of cortical surface potentials recorded in cat primary auditory cortex using thin film surface arrays: Comparisons with multi-unit data

BackgroundCurrent source density analysis of recordings from penetrating electrode arrays has traditionally been used to examine the layer- specific cortical activation and plastic changes associated with changed afferent input. We report on a related analysis, the second spatial derivative (SSD) of surface local field potentials (LFPs) recorded using custom designed thin-film polyimide substrate arrays. ResultsSSD analysis of tone- evoked LFPs generated from the auditory cortex under the recording array demonstrated a stereotypical single local minimum, often flanked by maxima on both the caudal and rostral sides. In contrast, tone-pips at frequencies not represented in the region under the array, but known (on the basis of normal tonotopic organization) to be represented caudal to the recording array, had a more complex pattern of many sources and sinks. Comparison with existing methodsCompared to traditional analysis of LFPs, SSD analysis produced a tonotopic map that was more similar to that obtained with multi-unit recordings in a normal-hearing animal. Additionally, the statistically significant decrease in the number of acoustically responsive cortical locations in partially deafened cats following 6 months of cochlear implant use compared to unstimulated cases observed with multi-unit data (p=0.04) was also observed with SSD analysis (p=0.02), but was not apparent using traditional analysis of LFPs (p=0.6). ConclusionsSSD analysis of surface LFPs from the thin-film array provides a rapid and robust method for examining the spatial distribution of cortical activity with improved spatial resolution compared to more traditional LFP recordings.

Differential Modification of Cortical and Thalamic Projections to Cat Primary Auditory Cortex Following Early- and Late-Onset Deafness.

Following sensory deprivation, primary somatosensory and visual cortices undergo crossmodal plasticity, which subserves the remaining modalities. However, controversy remains regarding the neuroplastic potential of primary auditory cortex (A1). To examine this, we identified cortical and thalamic projections to A1 in hearing cats and those with early- and late-onset deafness. Following early deafness, inputs from second auditory cortex (A2) are amplified, whereas the number originating in the dorsal zone (DZ) decreases. In addition, inputs from the dorsal medial geniculate nucleus (dMGN) increase, whereas those from the ventral division (vMGN) are reduced. In late-deaf cats, projections from the anterior auditory field (AAF) are amplified, whereas those from the DZ decrease. Additionally, in a subset of early- and late-deaf cats, area 17 and the lateral posterior nucleus (LP) of the visual thalamus project concurrently to A1. These results demonstrate that patterns of projections to A1 are modified following deafness, with statistically significant changes occurring within the auditory thalamus and some cortical areas. Moreover, we provide anatomical evidence for small-scale crossmodal changes in projections to A1 that differ between early- and late-onset deaf animals, suggesting that potential crossmodal activation of primary auditory cortex differs depending on the age of deafness onset.

Effects of deafness and cochlear implant use on temporal response characteristics in cat primary auditory cortex

We have previously shown that neonatal deafness of 7–13 months duration leads to loss of cochleotopy in the primary auditory cortex (AI) that can be reversed by cochlear implant use. Here we describe the effects of a similar duration of deafness and cochlear implant use on temporal processing. Specifically, we compared the temporal resolution of neurons in AI of young adult normal-hearing cats that were acutely deafened and implanted immediately prior to recording with that in three groups of neonatally deafened cats. One group of neonatally deafened cats received no chronic stimulation. The other two groups received up to 8 months of either low- or high-rate (50 or 500 pulses per second per electrode, respectively) stimulation from a clinical cochlear implant, initiated at 10 weeks of age. Deafness of 7–13 months duration had no effect on the duration of post-onset response suppression, latency, latency jitter, or the stimulus repetition rate at which units responded maximally (best repetition rate), but resulted in a statistically significant reduction in the ability of units to respond to every stimulus in a train (maximum following rate). None of the temporal response characteristics of the low-rate group differed from those in acutely deafened controls. In contrast, high-rate stimulation had diverse effects: it resulted in decreased suppression duration, longer latency and greater jitter relative to all other groups, and an increase in best repetition rate and cut-off rate relative to acutely deafened controls. The minimal effects of moderate-duration deafness on temporal processing in the present study are in contrast to its previously-reported pronounced effects on cochleotopy. Much longer periods of deafness have been reported to result in significant changes in temporal processing, in accord with the fact that duration of deafness is a major factor influencing outcome in human cochlear implantees.

Cross-correlations between three units in cat primary auditory cortex

Here we use a modification of the Joint-Peri-Stimulus-Time histogram (JPSTH) to investigate triple correlations between cat auditory cortex neurons. The modified procedure allowed the decomposition of the xy-pair correlation into a part that is due to the correlation of the x and y units with the trigger unit, and a remaining ‘pair correlation’. We analyzed 16 sets of 15-minute duration stationary spontaneous recordings in primary auditory cortex (AI) with between 11 and 14 electrodes from 2 arrays of 8 electrodes each that provided spontaneous firing rates above 0.22 sp/s and for which reliable frequency-tuning curves could be obtained and the characteristic frequency (CF) was estimated. Thus we evaluated 11,282 conditional cross-correlation functions.The predictor for the conditional cross-correlation, calculated on the assumption that the trigger unit had no effect on the xy-pair correlation but using the same fraction of xy spikes, was equal to the conventional pair-wise correlation function between units xy. The conditional correlation of the xy-pair due to correlation of the x and/or y unit with the trigger unit decreased with the geometric mean distance of the xy pair to the trigger unit, but was independent of the pair cross-correlation coefficient. The conditional pair correlation coefficient was estimated at 78% of the measured pair correlation coefficient. Assuming a geometric decreasing effect of activities of units on other electrodes on the conditional correlation, we estimated the potential contribution of a large number of contributing units on the measured pair correlation at 35–50 of that correlation. This suggests that conventionally measured pair correlations in auditory cortex under ketamine anesthesia overestimate the ‘true pair correlation’, likely resulting from massive common input, by potentially up to a factor 2.

Spontaneous firing rate changes in cat primary auditory cortex following long-term exposure to non-traumatic noise: Tinnitus without hearing loss?

Changes of neural activity in animal models have been correlated with tinnitus in humans. For instance, increased spontaneous firing rates (SFR), increased spontaneous neural synchrony, and cortical tonotopic map reorganization may underlie this phantom auditory percept. The aim of this study is to quantify the changes in SFR activity in the cat primary auditory cortex, after long-term exposure to different types of non-traumatic acoustic environments. For that purpose, four different groups of adult cats were exposed to moderate-level (~70dB SPL), behaviorally irrelevant sounds for several weeks to months, and their SFRs were compared with those in control cats. The sounds consisted of random multi-frequency tone pip ensembles with various bandwidths (2–4kHz, 4–20kHz, and a pair of third-octave bands centered at 4 and 16kHz), as well as a “factory noise”. Auditory brainstem response (ABR) thresholds, ABR wave 3 amplitudes at ~55 and 75dB SPL, and distortion product otoacoustic emission (DPOAE) amplitudes were unaffected by the exposure. However, we found that the SFR decreased within the exposure frequency range and increased outside the exposure range. This increased SFR for units with characteristic frequencies outside the exposure frequency range, which was slow to reverse after the exposure offset, suggests a mechanism for tinnitus in the absence of hearing loss.

Localization of single‐cell current sources based on extracellular potential patterns: the spike CSD method

Traditional current source density (tCSD) calculation method calculates neural current source distribution of extracellular (EC) potential patterns, thus providing important neurophysiological information. While the tCSD method is based on physical principles, it adopts some assumptions, which can not hold for single-cell activity. Consequently, tCSD method gives false results for single-cell activity. A new, spike CSD (sCSD) method has been developed, specifically designed to reveal CSD distribution of single cells during action potential generation. This method is based on the inverse solution of the Poisson-equation. The efficiency of the method is tested and demonstrated with simulations, and showed, that the sCSD method reconstructed the original CSD more precisely than the tCSD. The sCSD method is applied to EC spatial potential patterns of spikes, measured in cat primary auditory cortex with a 16-channel chronically implanted linear probe in vivo. Using our method, the cell-electrode distances were estimated and the spatio-temporal CSD distributions were reconstructed. The results suggested, that the new method is potentially useful in determining fine details of the spatio-temporal dynamics of spikes.

Differential representation of auditory categories between cell classes in primate auditory cortex

A comprehensive understanding of the neural mechanisms of cognitive function requires an understanding of how neural representations are transformed across different scales of neural organization: from within local microcircuits to across different brain areas. However, the neural transformations within the local microcircuits are poorly understood. Particularly, the role that two main cell classes of neurons in cortical microcircuits (i.e. pyramidal neurons and interneurons) have in auditory behaviour and cognition remains unknown. In this study, we tested the hypothesis that pyramidal cells and interneurons in the auditory cortex play a differential role in auditory categorization. To test this hypothesis, we recorded single-unit activity from the auditory cortex of rhesus monkeys while they categorized speech sounds. Based on the spike-waveform shape, a neuron was classified as either a narrow-spiking putative interneuron or a broad-spiking putative pyramidal neuron. We found that putative interneurons and pyramidal neurons in the auditory cortex differentially coded category information: interneurons were more selective for auditory categories than pyramidal neurons. These differences between cell classes may be an essential property of the neural computations underlying auditory categorization within the microcircuitry of the auditory cortex.

Correlation between neural discharges in cat primary auditory cortex and tone-detection behaviors

Understanding the physiological role of the auditory cortex (AC) in acoustic perception is an essential issue in auditory neuroscience. By comparing sound discrimination behaviors in animals before and after AC lesion, many studies have demonstrated that AC is necessary for the perceptual process of human vowels and animal vocalizations, but is not necessary to discriminate simple acoustic parameters such as sound onset, intensity and duration. Because a lesion study cannot fully reveal the function of AC under normal conditions, in this study, we combined electrophysiological recording and psychophysical experiments on the same animal to investigate whether AC is involved in a simple auditory task. We recorded the neural activities of the primary auditory cortex (A1) using implanted electrodes, while freely-moving cats performed a tone-detection task in which they were required to lick a metal tube to obtain a food reward after hearing a tone pip. The performance of the cats’ behavioral response increased with the increase of tone intensity, and the neural activities of A1 covaried with the behavioral performance. Also, whether the tone-detection behavior was interfered by a wideband noise was dependent on whether the tone-evoked neural response was masked by the noise-evoked response. Our results did not support that A1 neurons directly associate with the cat's behavioral decision; instead, they may mainly generate a neural representation of stimulus amplitude for further processing to determine whether a tone occurred or not.

Spectrotemporal Processing in Spectral Tuning Modules of Cat Primary Auditory Cortex

Spectral integration properties show topographical order in cat primary auditory cortex (AI). Along the iso-frequency domain, regions with predominantly narrowly tuned (NT) neurons are segregated from regions with more broadly tuned (BT) neurons, forming distinct processing modules. Despite their prominent spatial segregation, spectrotemporal processing has not been compared for these regions. We identified these NT and BT regions with broad-band ripple stimuli and characterized processing differences between them using both spectrotemporal receptive fields (STRFs) and nonlinear stimulus/firing rate transformations. The durations of STRF excitatory and inhibitory subfields were shorter and the best temporal modulation frequencies were higher for BT neurons than for NT neurons. For NT neurons, the bandwidth of excitatory and inhibitory subfields was matched, whereas for BT neurons it was not. Phase locking and feature selectivity were higher for NT neurons. Properties of the nonlinearities showed only slight differences across the bandwidth modules. These results indicate fundamental differences in spectrotemporal preferences - and thus distinct physiological functions - for neurons in BT and NT spectral integration modules. However, some global processing aspects, such as spectrotemporal interactions and nonlinear input/output behavior, appear to be similar for both neuronal subgroups. The findings suggest that spectral integration modules in AI differ in what specific stimulus aspects are processed, but they are similar in the manner in which stimulus information is processed.

Neuronal activation times to simple, complex, and natural sounds in cat primary and nonprimary auditory cortex

Interactions between living organisms and the environment are commonly regulated by accurate and timely processing of sensory signals. Hence, behavioral response engagement by an organism is typically constrained by the arrival time of sensory information to the brain. While psychophysical response latencies to acoustic information have been investigated, little is known about how variations in neuronal response time relate to sensory signal characteristics. Consequently, the primary objective of the present investigation was to determine the pattern of neuronal activation induced by simple (pure tones), complex (noise bursts and frequency modulated sweeps), and natural (conspecific vocalizations) acoustic signals of different durations in cat auditory cortex. Our analysis revealed three major cortical response characteristics. First, latency measures systematically increase in an antero-dorsal to postero-ventral direction among regions of auditory cortex. Second, complex acoustic stimuli reliably provoke faster neuronal response engagement than simple stimuli. Third, variations in neuronal response time induced by changes in stimulus duration are dependent on acoustic spectral features. Collectively, these results demonstrate that acoustic signals, regardless of complexity, induce a directional pattern of activation in auditory cortex.

Comparison of LFP-Based and Spike-Based Spectro-Temporal Receptive Fields and Cross-Correlation in Cat Primary Auditory Cortex

Multi-electrode array recordings of spike and local field potential (LFP) activity were made from primary auditory cortex of 12 normal hearing, ketamine-anesthetized cats. We evaluated 259 spectro-temporal receptive fields (STRFs) and 492 frequency-tuning curves (FTCs) based on LFPs and spikes simultaneously recorded on the same electrode. We compared their characteristic frequency (CF) gradients and their cross-correlation distances. The CF gradient for spike-based FTCs was about twice that for 2–40 Hz-filtered LFP-based FTCs, indicating greatly reduced frequency selectivity for LFPs. We also present comparisons for LFPs band-pass filtered between 4–8 Hz, 8–16 Hz and 16–40 Hz, with spike-based STRFs, on the basis of their marginal frequency distributions. We find on average a significantly larger correlation between the spike based marginal frequency distributions and those based on the 16–40 Hz filtered LFP, compared to those based on the 4–8 Hz, 8–16 Hz and 2–40 Hz filtered LFP. This suggests greater frequency specificity for the 16–40 Hz LFPs compared to those of lower frequency content. For spontaneous LFP and spike activity we evaluated 1373 pair correlations for pairs with >200 spikes in 900 s per electrode. Peak correlation-coefficient space constants were similar for the 2–40 Hz filtered LFP (5.5 mm) and the 16–40 Hz LFP (7.4 mm), whereas for spike-pair correlations it was about half that, at 3.2 mm. Comparing spike-pairs with 2–40 Hz (and 16–40 Hz) LFP-pair correlations showed that about 16% (9%) of the variance in the spike-pair correlations could be explained from LFP-pair correlations recorded on the same electrodes within the same electrode array. This larger correlation distance combined with the reduced CF gradient and much broader frequency selectivity suggests that LFPs are not a substitute for spike activity in primary auditory cortex.

Auditory Neuroscience: Temporal Anticipation Enhances Cortical Processing

A recent study shows that expectation about the timing of behaviorally-relevant sounds enhances the responses of neurons in the primary auditory cortex and improves the accuracy and speed with which animals respond to those sounds.

Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats

It is well known that the post-natal loss of sensory input in one modality can result in crossmodal reorganization of the deprived cortical areas, but deafness fails to induce crossmodal effects in cat primary auditory cortex (A1). Because the core auditory regions (A1, and anterior auditory field AAF) are arranged as separate, parallel processors, it cannot be assumed that early-deafness affects one in the same manner as the other. The present experiments were conducted to determine if crossmodal effects occur in the anterior auditory field (AAF). Using mature cats (n = 3), ototoxically deafened postnatally, single-unit recordings were made in the gyral and sulcal portions of the AAF. In contrast to the auditory responsivity found in the hearing controls, none of the neurons in early-deafened AAF were activated by auditory stimulation. Instead, the majority (78%) were activated by somatosensory cues, while fewer were driven by visual stimulation (44%; values include unisensory and bimodal neurons). Somatosensory responses could be activated from all locations on the body surface but most often occurred on the head, were often bilateral (e.g., occupied portions of both sides of the body), and were primarily excited by low-threshold hair receptors. Visual receptive fields were large, collectively represented the contralateral visual field, and exhibited conventional response properties such as movement direction and velocity preferences. These results indicate that, following post-natal deafness, both somatosensory and visual modalities participate in crossmodal reinnervation of the AAF, consistent with the growing literature that documents deafness-induced crossmodal plasticity outside A1.

Dual Mechanism of Neuronal Ensemble Inhibition in Primary Auditory Cortex

Inhibition plays an essential role in shaping and refining the brain's representation of sensory stimulus attributes. In primary auditory cortex (A1), so-called "sideband" inhibition helps to sharpen the tuning of local neuronal responses. Several distinct types of anatomical circuitry could underlie sideband inhibition, including direct thalamocortical (TC) afferents, as well as indirect intracortical mechanisms. The goal of the present study was to characterize sideband inhibition in A1 and to determine its mechanism by analyzing laminar profiles of neuronal ensemble activity. Our results indicate that both lemniscal and nonlemniscal TC afferents play a role in inhibitory responses via feedforward inhibition and oscillatory phase reset, respectively. We propose that the dynamic modulation of excitability in A1 due to the phase reset of ongoing oscillations may alter the tuning of local neuronal ensembles and can be regarded as a flexible overlay on the more obligatory system of lemniscal feedforward type responses.

Distinct core thalamocortical pathways to central and dorsal primary auditory cortex

The cat primary auditory cortex (AI) is usually assumed to form one continuous functional region. However, the dorsal and central parts of the AI iso-frequency domain contain neurons that have distinct response properties to acoustic stimuli. In this study, we asked whether neurons projecting to dorsal versus central regions of AI originate in different parts of the medial geniculate body (MGB). Spike rate responses to variations in the sound level and frequency of pure tones were used to measure characteristic frequency (CF) and frequency resolution. These were mapped with high spatial density in order to place retrograde tracers into matching frequency regions of the central narrow-band region (cNB) and dorsal AI. Labeled neurons projecting to these two parts of AI were concentrated in the middle and rostral thirds of the MGB, respectively. There was little evidence that differences in dorsal and central AI function could be due to convergent input from cells outside the ventral division of the MGB (MGBv). Instead, inputs arising from different locations along the caudal-to-rostral dimension of MGBv represent potential sources of response differences between central and dorsal sub-regions of AI.

GABAergic organization of the auditory cortex in the mustached bat (Pteronotus p. parnellii)

The structure and distribution of neurons and axon terminals (puncta) immunostained for gamma-aminobutyric acid (GABA) in the parietotemporal neocortex of the mustached bat (Pteronotus p. parnellii) was studied. The types of GABAergic neurons and puncta (putative terminals) were analyzed, and the immunocytochemical patterns were compared to those in cat auditory cortex (AC). The classic map of mustached bat primary auditory cortex (AI) corresponds to a belt of granular six-layered cortex on the temporal convexity. This area encompasses the Doppler-shifted constant frequency 60 kHz domain (DSCF) described in physiological investigations, as well as its flanking, low-frequency, posterior field (AIp) and the anterior high-frequency region (AIa). Many types of GABAergic neurons correspond to those in cat primary AC. However, the bat had a significantly lower proportion of such cells in five of the six layers. The classes of GABAergic neurons in most layers were small, medium-sized, and large multipolar cells, and bipolar and bitufted neurons. Types found in only one or two layers included horizontal cells (layers I and VI) or extraverted multipolar neurons (layer II). Only layer IV had comparable percentages (∼26%), suggesting that the GABAergic influence on lemniscal thalamocortical input is conserved phylogenetically. While the cellular basis for GABAergic cortical processing may reflect shared neural circuits and common modes of inhibitory processing, laminar differences could underlie adaptations specific to microchioptera.

Columnar connectivity and laminar processing in cat primary auditory cortex.

BackgroundRadial intra- and interlaminar connections form a basic microcircuit in primary auditory cortex (AI) that extracts acoustic information and distributes it to cortical and subcortical networks. Though the structure of this microcircuit is known, we do not know how the functional connectivity between layers relates to laminar processing.Methodology/Principal FindingsWe studied the relationships between functional connectivity and receptive field properties in this columnar microcircuit by simultaneously recording from single neurons in cat AI in response to broadband dynamic moving ripple stimuli. We used spectrotemporal receptive fields (STRFs) to estimate the relationship between receptive field parameters and the functional connectivity between pairs of neurons. Interlaminar connectivity obtained through cross-covariance analysis reflected a consistent pattern of information flow from thalamic input layers to cortical output layers. Connection strength and STRF similarity were greatest for intralaminar neuron pairs and in supragranular layers and weaker for interlaminar projections. Interlaminar connection strength co-varied with several STRF parameters: feature selectivity, phase locking to the stimulus envelope, best temporal modulation frequency, and best spectral modulation frequency. Connectivity properties and receptive field relationships differed for vertical and horizontal connections.Conclusions/SignificanceThus, the mode of local processing in supragranular layers differs from that in infragranular layers. Therefore, specific connectivity patterns in the auditory cortex shape the flow of information and constrain how spectrotemporal processing transformations progress in the canonical columnar auditory microcircuit.