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Spontaneous burst firing in cat primary auditory cortex: age and depth dependence and its effect on neural interaction measures.

1. Neural activity was recorded with two independent electrodes separated by 0.5-2 mm, aligned in parallel, and advanced perpendicular to the surface of the cat auditory cortex. Because the experiments were part of a study into laminar interaction the difference in recording depths for the two independently movable electrodes was never > 100 microns. Multi-unit activity on each electrode was separated on-line into single-unit spike-trains with a maximum variance spike sorting algorithm. Off-line controls on the quality of the spike-train separation were routinely performed. The first aim of this study was to describe the age dependence of spontaneous burst firing and to explore if and how it could be explained by age dependent changes in firing rate. The second aim was to investigate a potential layer dependence on burst firing. The third aim was to describe the effect of burst-removal procedures on the shape, strength, and width of the cross-correlogram and to investigate whether an age dependence in burst firing might account for the previously reported age dependence in correlation strengths. 2. Recordings were made from 237 single units from primary auditory cortex in nine adult cats and from 67 units in seven kittens age 10-52 days. The incidence of burst firing as a function of firing rate, age and depth of recording and unit characteristic frequency was investigated. In addition the effect of burst firing on the strength and width of the central peak in 471 neural pair correlograms was analyzed. 3. Burst firing could be distinguished at many different time scales; bursts lasting of the order of 10 s contained bursts with durations of the order of 1 s, which in turn contained bursts of 30-50-ms duration. The analysis in this paper was restricted to the short-duration bursts. 4. Burst firing on the short-time scale of 50 ms was characterized by relatively well defined intervals between the first two spikes (3-15 ms) followed by higher-order intervals with large spread (range 4-50 ms) but with increasing modal interval value. The typical adult five-spike burst template featured spikes at 0, 3.3, 14.6, 27.2, and 34.8 ms. Burst with fewer spikes showed larger intervals between the first three spikes. 5. The probability of occurrence of isolated spikes, pairs, triplets, etc. showed a power-law dependence on firing rate with a coefficient that was significantly lower than expected under Poisson firing conditions.(ABSTRACT TRUNCATED AT 400 WORDS)

Action Potentials↗

Sound-induced changes of infraslow brain potential fluctuations in the medial geniculate nucleus and primary auditory cortex in anaesthetized rats.

Recent publications indicate the presence of infraslow activity (<0.5 Hz) in subcortical and cortical sites of the auditory system of the brain. It has been reported that this activity might be sensitive to acoustic stimuli. Yet the dynamics of infraslow brain potential (ISBP) fluctuations in these structures and their potential sensitivity to auditory stimuli are unknown. The present study was performed in order to test the hypothesis that extracellular ISBP activity in the medial geniculate nucleus (MGN) and the primary auditory cortex (A1) responds concurrently to acoustic stimuli. The experimental subjects were 5 adult rats with chronic stereotaxic electrodes implanted in MGN and A1. The animals were anesthetized and recordings were made in both sites during both silence and rhythmical acoustic stimulation. Our results support the hypothesis that these fluctuations are sensitive to acoustic stimuli. There were similar changes in ISBP activity in the MGN and A1 in response to rhythmic acoustic stimulation. Specifically, there were significant increases in the frequency range of seconds. Based on these findings, we suggest that sound-correlated changes in infraslow activity in the range of seconds in the MGN and A1 reflect specific mechanisms of neural processing of acoustic information in the auditory system of the brain.

Acoustic Stimulation↗

Response adaptation to broadband sounds in primary auditory cortex of the awake ferret.

Driven by previous reports of adaptation to persistent stimuli in other brain regions, we investigated adaptive effects in the Primary Auditory Cortex of awake non-behaving ferrets (Mustela putorius furo). Electrophysiological data was obtained in response to the presentation of auditory gratings with a structured spectro-temporal envelope of varying bandwidth which had repeated transitions between low and high modulation depths. The responses were analyzed in terms of the evoked spike rates and in terms of the degree of phase locking to the modulation. We found two populations of cells, both of which showed adaptation in the traditional sense. For one population, we also found a second order of adaptation--i.e., adaptation of the adaptation. This suggests the existence of at least two coding strategies which differ in the weight placed on sensory context.

Acoustic Stimulation↗

Single unit activity in the auditory cortex and the medial geniculate body of the rhesus monkey: behavioral modulation.

Three Rhesus monkeys were trained to respond to a given auditory signal, the nature of which could be predicted from a preceding visual stimulus. The activity of 28 units in the auditory cortex and 53 units in the Medial Geniculate Body (MGB) of the monkey was recorded during task-performance conditions, as well as in the non-performance conditions. The activity of about one third of the cortical and MGB units was independent of the behaving status of the animal. In other units, the response to an auditory signal delivered during task-performance conditions as compared to the response recorded during non-performance periods was either augmented or attenuated. Furthermore, it was found that the spontaneous activity of most of the MGB and cortical units was continuously affected by either an excitatory or an inhibitory input, activated by the behavioral state. The temporal characteristics of behavioral modulation were studied by computing an amplification curve for all MGB units characterized by a 'through stimulus excitation' type of response. Analysis of these curves together with the behavioral effect on the spontaneous activity allows the suggestion of possible mechanisms by which the behavioral state of the monkey modulates the activity in the thalamocortical segment of the auditory system.

Animals↗

Expansion of the tonotopic area in the auditory cortex of the blind.

A part of the core area of the auditory cortex was examined in nine blind and 10 sighted individuals by magnetic source imaging and was found to be enlarged by a factor of 1.8 in the blind compared with the sighted humans. Moreover, the latency of the N1m component of the auditory-evoked magnetic response was significantly decreased in the blind. The development of use-dependent cortical reorganization may be a consequence of the absence of visual input in combination with enhanced auditory activity generated by the long-term concentration by blind individuals on nonvisual cues to interact appropriately with the environment. It is consistent with and well suited to mediate the demonstrated increased ability of the blind to accurately localize acoustic sources in peripheral auditory fields and to decode speech.

Acoustic Stimulation↗

Changes in cat primary auditory cortex after minor-to-moderate pure-tone induced hearing loss.

In this paper we present findings in the primary auditory cortex of cats exposed for 2 h to a 115 dB SPL, 6 kHz tone at 36 days, 56 days or 118 days after birth. We evaluate the effects of age at exposure, amount of hearing loss, and time after induction of trauma on the functional reorganization of the cortical tonotopic map. We found a fairly sharp demarcation in the amount of hearing loss (20-25 dB) that caused cortical reorganization. For localized hearing losses, unmasking of excitatory contributions of neighboring frequency regions was found. For cats showing reorganization of the tonotopic map, the frequency-tuning curve bandwidth at 20 dB above threshold at CF (BW(20dB)) increased with increasing threshold at CF. Threshold at CF, and BW(20dB) increased with time after exposure. Minimum spike latency was initially increased, but subsequently decreased with time after exposure at a rate that was two times faster in cats with reorganized cortex than in cats with normal tonotopic maps, to reach the same asymptotic value. Thresholds at CF were correlated with the peripheral hearing loss at near CF frequencies as estimated from ABR measurements. The correlation between BW(20dB) and CF threshold suggests that part of the reorganization could be due to 'residual' sensitivity of the high frequency neurons to not-affected lower or higher frequencies. However, for CFs above 6 kHz, the BW(20dB) for cats with reorganization of the tonotopic map was significantly lower (on average 0.3 octave, P<0.05) than for cats with normal tonotopic maps. This is not what one would expect in cases of pseudo-plasticity characterized by concurrent shifts in BW(20dB) and CF as a result of residual sensitivity to lower frequencies.

Action Potentials↗

Stimulus-invariant processing and spectrotemporal reverse correlation in primary auditory cortex.

The spectrotemporal receptive field (STRF) provides a versatile and integrated, spectral and temporal, functional characterization of single cells in primary auditory cortex (AI). In this paper, we explore the origin of, and relationship between, different ways of measuring and analyzing an STRF. We demonstrate that STRFs measured using a spectrotemporally diverse array of broadband stimuli-such as dynamic ripples, spectrotemporally white noise, and temporally orthogonal ripple combinations (TORCs)-are very similar, confirming earlier findings that the STRF is a robust linear descriptor of the cell. We also present a new deterministic analysis framework that employs the Fourier series to describe the spectrotemporal modulations contained in the stimuli and responses. Additional insights into the STRF measurements, including the nature and interpretation of measurement errors, is presented using the Fourier transform, coupled to singular-value decomposition (SVD), and variability analyses including bootstrap. The results promote the utility of the STRF as a core functional descriptor of neurons in AI.

Acoustic Stimulation↗

Spatial processing in human auditory cortex: the effects of 3D, ITD, and ILD stimulation techniques.

Here, the perception of auditory spatial information as indexed by behavioral measures is linked to brain dynamics as reflected by the N1m response recorded with whole-head magnetoencephalography (MEG). Broadband noise stimuli with realistic spatial cues corresponding to eight direction angles in the horizontal plane were constructed via custom-made, individualized binaural recordings (BAR) and generic head-related transfer functions (HRTF). For comparison purposes, stimuli with impoverished acoustical cues were created via interaural time and level differences (ITDs and ILDs) and their combinations. MEG recordings in ten subjects revealed that the amplitude and the latency of the N1m exhibits directional tuning to sound location, with the amplitude of the right-hemispheric N1m being particularly sensitive to the amount of spatial cues in the stimuli. The BAR, HRTF, and combined ITD + ILD stimuli resulted both in a larger dynamic range and in a more systematic distribution of the N1m amplitude across stimulus angle than did the ITD or ILD stimuli alone. Further, the right-hemispheric source loci of the N1m responses for the BAR and HRTF stimuli were anterior to those for the ITD and ILD stimuli. In behavioral tests, we measured the ability of the subjects to localize BAR and HRTF stimuli in terms of azimuthal error and front-back confusions. We found that behavioral performance correlated positively with the amplitude of the N1m. Thus, the activity taking place already in the auditory cortex predicts behavioral sound detection of spatial stimuli, and the amount of spatial cues embedded in the signal are reflected in the activity of this brain area.

Acoustic Stimulation↗

Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex.

It has been suggested that "call-selective" neurons may play an important role in the encoding of vocalizations in primary auditory cortex (A1). For example, marmoset A1 neurons often respond more vigorously to natural than to time-reversed twitter calls, although the spectral energy distribution in the natural and time-reversed signals is the same. Neurons recorded in cat A1, in contrast, showed no such selectivity for natural marmoset calls. To investigate whether call selectivity in A1 can arise purely as a result of auditory experience, we recorded responses to marmoset calls in A1 of naive ferrets, as well as in ferrets that had been trained to recognize these natural marmoset calls. We found that training did not induce call selectivity for the trained vocalizations in A1. However, although ferret A1 neurons were not call selective, they efficiently represented the vocalizations through temporal pattern codes, and trained animals recognized marmoset twitters with a high degree of accuracy. These temporal patterns needed to be analyzed at timescales of 10-50 ms to ensure efficient decoding. Training led to a substantial increase in the amount of information transmitted by these temporal discharge patterns, but the fundamental nature of the temporal pattern code remained unaltered. These results emphasize the importance of temporal discharge patterns and cast doubt on the functional significance of call-selective neurons in the processing of animal communication sounds at the level of A1.

Acoustic Stimulation↗

Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections.

The development of the different, highly specialized regions of the mammalian cerebral cortex depends in part on neural activity, either intrinsic spontaneous activity or externally driven sensory activity. To determine whether patterned sensory activity instructs the development of intrinsic cortical circuitry, we have experimentally altered the modality of sensory inputs to cerebral cortex. Neonatal diversion of retinal axons to the auditory thalamus (cross-modal rewiring) results in a primary auditory cortex (AI) that resembles visual cortex in its response properties and topography (Roe et al., 1990, 1992). To test the hypothesis that the visual response properties are created by a visually driven reorganization of auditory cortical circuitry, we investigated the effect of early visual experience on the development of intrinsic, horizontal connections within AI. Horizontal connections are likely to play an important role in the construction of visual response properties in AI as they do in visual cortex. Here we show that early visual inputs to auditory thalamus can reorganize horizontal connections in AI, causing both an increase in their extent and a change in pattern, so that projections are not restricted to the isofrequency axis, but extend in a more isotropic pattern around the injection site. Thus, changing afferent modality, without altering the source of the thalamocortical axons, can profoundly alter cortical circuitry. Similar changes may underlie cortical compensatory processes in deaf or blind humans and may also have played a role in the parcellation of neocortex during mammalian evolution.

Afferent Pathways↗

Codes for sound-source location in nontonotopic auditory cortex.

We evaluated two hypothetical codes for sound-source location in the auditory cortex. The topographical code assumed that single neurons are selective for particular locations and that sound-source locations are coded by the cortical location of small populations of maximally activated neurons. The distributed code assumed that the responses of individual neurons can carry information about locations throughout 360 degrees of azimuth and that accurate sound localization derives from information that is distributed across large populations of such panoramic neurons. We recorded from single units in the anterior ectosylvian sulcus area (area AES) and in area A2 of alpha-chloralose-anesthetized cats. Results obtained in the two areas were essentially equivalent. Noise bursts were presented from loudspeakers spaced in 20 degrees intervals of azimuth throughout 360 degrees of the horizontal plane. Spike counts of the majority of units were modulated >50% by changes in sound-source azimuth. Nevertheless, sound-source locations that produced greater than half-maximal spike counts often spanned >180 degrees of azimuth. The spatial selectivity of units tended to broaden and, often, to shift in azimuth as sound pressure levels (SPLs) were increased to a moderate level. We sometimes saw systematic changes in spatial tuning along segments of electrode tracks as long as 1.5 mm but such progressions were not evident at higher sound levels. Moderate-level sounds presented anywhere in the contralateral hemifield produced greater than half-maximal activation of nearly all units. These results are not consistent with the hypothesis of a topographic code. We used an artificial-neural-network algorithm to recognize spike patterns and, thereby, infer the locations of sound sources. Network input consisted of spike density functions formed by averages of responses to eight stimulus repetitions. Information carried in the responses of single units permitted reasonable estimates of sound-source locations throughout 360 degrees of azimuth. The most accurate units exhibited median errors in localization of <25 degrees, meaning that the network output fell within 25 degrees of the correct location on half of the trials. Spike patterns tended to vary with stimulus SPL, but level-invariant features of patterns permitted estimates of locations of sound sources that varied through 20-dB ranges. Sound localization based on spike patterns that preserved details of spike timing consistently was more accurate than localization based on spike counts alone. These results support the hypothesis that sound-source locations are represented by a distributed code and that individual neurons are, in effect, panoramic localizers.

Action Potentials↗

The masking level difference in chinchilla auditory cortex. Effects of inner hair cell loss.

The purpose of the present study was to investigate responses from the unanesthetized chinchilla auditory cortex (AC) to conditions producing a masking level difference (MLD) in perceptual studies, both before and after inner hair cell (IHC) loss caused by carboplatin. Tungsten electrodes were chronically implanted in the right AC (active) and anterior cranium (common) in six adult chinchillas. Following a recovery period, AC responses were obtained from the unanesthetized animal placed in a passive restraint. Toneburst input/output functions were obtained. Tonebursts (500 Hz) ranged from 0 to 80 dB pSPL, in 10 dB steps, and were presented to the left ear, the right ear, binaural (in-phase) and binaural (out-of-phase). For the MLD series, responses to 70 dB pSPL, 500 Hz tonebursts and a continuous broadband noise (40-90 dB SPL, in 5 dB steps) were studied. Three MLD versus non-MLD conditions were obtained: SpiN0/S0N0, SLN0/SLNL, and SRN0/SRNR. Following baseline data collection, each animal was given 75 mg/kg carboplatin intraperitoneally. Four to five weeks later, the electrophysiology protocol was followed again. At 5 weeks post-carboplatin, the animals were sacrificed, the cochleas were harvested, and cochleograms (hair cell loss across cochlear place) were constructed. For all conditions, response latencies increased and amplitudes decreased with decreasing toneburst level and increasing level of masking noise. Masked AC response thresholds were higher (better) for the MLD conditions than their respective non-MLD conditions. AC response latencies across masking noise level did not appear to vary systematically across conditions. Under some conditions, the MLD conditions showed larger amplitudes than their respective non-MLD conditions for equivalent masker levels. Post-carboplatin, cochleograms showed moderate IHC loss (on average, approximately 40% loss in apex) with minimal outer hair cell loss. The differences in MLD versus non-MLD conditions in terms of masked threshold and response amplitude were often reduced post-carboplatin.

Acoustic Stimulation↗

Functional magnetic resonance imaging assessment of the human brain auditory cortex response to increasing word presentation rates.

In an investigation of the auditory cortex response to speech, six subjects were studied using echo-planar functional magnetic resonance imaging (fMRI) at 2.1T. The subjects were asked to listen to English nouns presented at various rates ranging from 0 words per minute (wpm) to 130 wpm while fMRI images encompassing their primary and posterior superior secondary auditory cortices were acquired. An asymmetric spin echo imaging sequence was used with an induced T2 weighting of 50 ms to allow for transverse relaxation effects. Images were acquired in two or four axial-oblique slices with a repetition time of 3.75 or 7.5 s, in plane resolution of 6 x 3 mm, and a slice thickness of 5 mm. Localized activation centered over grey matter was consistently observed in all subjects in the transverse temporal gyrus (TTG), the transverse temporal sulcus (TTS), and the posterior superior aspect of the superior temporal gyrus (STG). The total activate volume and the integrated signal response in bilateral primary and posterior superior secondary auditory cortices increased with increasing rate of word presentation, peaking at 90 wpm (with some intersubject variability) with a subsequent fall at 130 wpm. There were no significant differences in the rate dependence of the signal response in bilateral primary and bilateral posterior superior secondary auditory cortices (P < 0.05).

Adult↗

Serial and parallel processing in the human auditory cortex: a magnetoencephalographic study.

Although anatomical, histochemical and electrophysiological findings in both animals and humans have suggested a parallel and serial mode of auditory processing, precise activation timings of each cortical area are not well known, especially in humans. We investigated the timing of arrival of signals to multiple cortical areas using magnetoencephalography in humans. Following click stimuli applied to the left ear, activations were found in six cortical areas in the right hemisphere: the posteromedial part of Heschl's gyrus (HG) corresponding to the primary auditory cortex (PAC), the anterolateral part of the HG region on or posterior to the transverse sulcus, the posterior parietal cortex (PPC), posterior and anterior parts of the superior temporal gyrus (STG), and the planum temporale (PT). The mean onset latencies of each cortical activity were 17.1, 21.2, 25.3, 26.2, 30.9 and 47.6 ms respectively. These results suggested a serial model of auditory processing along the medio-lateral axis of the supratemporal plane and, in addition, implied the existence of several parallel streams running postero-superiorly (from the PAC to the belt region and then to the posterior STG, PPC or PT) and anteriorly (PAC-belt-anterior STG).

Adult↗

Processing of changes in visual speech in the human auditory cortex.

Seeing a talker's articulatory gestures may affect the observer's auditory speech percept. Observing congruent articulatory gestures may enhance the recognition of speech sounds [J. Acoust. Soc. Am. 26 (1954) 212], whereas observing incongruent gestures may change the auditory percept phonetically as occurs in the McGurk effect [Nature 264 (1976) 746]. For example, simultaneous acoustic /ba/ and visual /ga/ are usually heard as /da/. We studied cortical processing of occasional changes in audiovisual and visual speech stimuli with magnetoencephalography. In the audiovisual experiment congruent (acoustic /iti/, visual /iti/) and incongruent (acoustic /ipi/, visual /iti/) audiovisual stimuli, which were both perceived as /iti/, were presented among congruent /ipi/ (acoustic /ipi/, visual /ipi/) stimuli. In the visual experiment only the visual components of these stimuli were presented. A visual change both in audiovisual and visual experiments activated supratemporal auditory cortices bilaterally. The auditory cortex activation to a visual change occurred later in the visual than in the audiovisual experiment, suggesting that interaction between modalities accelerates the detection of visual change in speech.

Acoustic Stimulation↗

Modulation of cochlear hair cells by the auditory cortex in the mustached bat.

The corticofugal (descending) auditory system forms multiple feedback loops, and adjusts and improves auditory signal processing in the subcortical auditory nuclei. However, the mechanism by which the corticofugal system modulates cochlear hair cells has been unexplored. We found that electric stimulation of cortical neurons via the corticofugal system modulates cochlear hair cells in a highly specific way according to the relationship in terms of best frequency between cortical neurons and hair cells. Such frequency-specific effects can be explained by selective corticofugal modulation of individual olivocochlear efferent fibers.

Animals↗

Measurement of regional cerebral blood flow and accentuation of the primary auditory cortex with single photon emission computed tomography.

Conventional brain scanning uses polar tracers which do not penetrate the normal blood-brain barrier. Radiolabeled amines like 123-iodoamphetamine (IMP) cross the barrier to inhibit serotonin and norepinephrine in synaptosomes. Studies of cerebral perfusion and function seem to be successful with such labeling. We advance the hypothesis for an increased IMP uptake in the stimulated primary auditory cortex. The method of single photon emission computed tomography (SPECT) is described. We have also been able to demonstrate marking of the primary auditory cortex by an increased amphetamine input in 6 out of 15 cases during stimulation by white noise.

Acoustic Stimulation↗

[Effect of penicillin on the discrimination function of the auditory cortex neurons in the cat].

Responses and receptive fields of neurons in auditory cortex (AI) were studied in acute nembutal-anaesthetized cats before and during ionophoretic application of penicillin. Frequency and duration of impulse responses to tone bursts were increased during application in the majority (83%) of neurons. Increase of receptive fields and decline of frequency selectivity were found in 80% of neurons. The data obtained are regarded as proofs of decisive role of GABA-ergic inhibition in formation of functional receptive fields of auditory cortical neurons.

Animals↗