Columnar organization and reciprocity of commissural connections in cat primary auditory cortex (AI)

The laminar distribution and reciprocity of commissural axon terminals and cells of origin in cat primary auditory cortex (AI) were studied after injections of tritiated proline combined with horseradish peroxidase in the middle ectosylvian gyrus. Terminal fields were found in every cortical layer in the contralateral AI, and they were characterized quantitatively. The largest concentration of silver grains was in layer III (about 25% of the total number of silver grains) and, to a lesser extent, in layers V, VI, and I (some 18% of the total in each layer). The labeling in layer I was concentrated in its deeper half, while the labeling in the other layers was more homogeneous. Layer IV had the least labeling, followed by layer II, each receiving about 10% of the total. The labeling was always heaviest over the neuropil and lightest over neuronal perikarya. Commissural terminal fields formed radial patches oriented perpendicularly to the pia, and averaging 543 micron in width. There was consistently three times more silver grains in a patch than in an inter-patch area. However, the number of silver grains in an inter-patch area was always significantly above background, indicating a possible commissural projection to these zones as well. The patches of commissural terminal fields formed bands oriented across AI and running in a caudoventral to rostrodorsal direction. Strict reciprocity between the commissural cells of origin and terminal fields was not found at the light microscopic level when adjacent sections, corrected for differential shrinkage, were compared. Often, patches of terminal fields were free of retrogradely labeled cells and, conversely, there were patches of labeled cells without an overlying commissural terminal field. The terminal fields connected homotopic regions of the contralateral AI, and every region of AI received commissural innervation, unlike the primary somatic sensory and visual cortex, where large zones receive only a few commissural afferents. The more complete pattern of interhemispheric connectivity in auditory cortex is in contrast to the less continuous commissural representation in other sensory neocortical fields. Perhaps this pattern contributes to the anatomical representation of binaurality in auditory cortex.     

The auditory steady state response: Far-field recordings from the chinchilla

Abstract

Objective: Previous studies in our lab have found that the presentation of multiple ASSR-generating stimuli results in a decrease in ASSR amplitude when recorded from an electrode implanted in the chinchilla inferior colliculus. The purpose of the present experiment was to determine whether this same effect occurs in far-field recordings, i.e. recordings similar to those made in human subjects. The effect of inhalant anesthesia on ASSR amplitude in response to multiple stimuli was also investigated. Design: Stimuli consisted of three sinusoidally-amplitude modulated tones with carrier/modulation frequencies of (1/.095 kHz), (2/.1 kHz), or (4/.107 kHz). The modulated carriers were presented to the right ear either alone or in combination, while recordings were made from subdermal needle electrodes placed on the head. Study sample: Nine adult chinchillas. Results: A 20%–70% decrease in the response amplitude with the presentation of multiple ASSR-generating stimuli was found, which depended on both carrier frequency as well as stimulus pairing. In general, both the ASSR and the noise floor were reduced under anesthesia. Conclusions: The time savings obtained from presenting multiple stimuli simultaneously may not be as great as initially predicted, as the time saving is at least partially offset by the observed amplitude reduction.     

Comparison between local field potentials and unit cluster activity in primary auditory cortex and anterior auditory field in the cat

Multi-unit (MU) activity and local field potentials (LFP) were simultaneously recorded from 161 sites in the middle cortical layers of the primary auditory cortex (AI) and the anterior auditory field (AAF) in 51 cats. Responses were obtained for frequencies between 625 Hz and 40 kHz, at intensities from 75 dB SPL to threshold. We compared the response properties of MU activity and LFP triggers, in terms of characteristic frequency (CF), threshold at CF, minimum latency and frequency tuning-curve bandwidth 20 dB above threshold. On average, thresholds at CF were significantly lower for LFP events than those for MU spikes (4.6 dB for AI, and 3 dB for AAF). Minimum latencies were significantly shorter for LFP events than for MU spikes (1.5 ms in AI, and 1.7 ms in AAF). Frequency tuning curves were significantly broader for LFP events than those for MU spikes (1.0 octave in AI, and 1.3 octaves in AAF). In contrast, the CF was not significantly different between LFP events and MU spikes. The LFP results indicate that cortical neurons receive convergent sub-cortical inputs from a broad frequency range. The sharper tuning curves for MU activity compared to those of LFP events are likely the result of intracortical inhibitory processes.     

Response properties of units in the posterior auditory field deprived of input from the ipsilateral primary auditory cortex

The influence of the ipsilateral primary auditory field (Al) on the response properties of neurons in the posterior auditory field (Field P) was examined in three cats anesthetized with sodium pentobarbital. Rate/level functions were obtained, by extracellular recording, from single units in Field P before (n = 38) and after (n = 50) subpial aspiration of AI. The ablations were primarily confined to the medial ectosylvian gyrus, although in one case extended into the high-frequency portion of the anterior auditory field. Comparisons between the behavior of units isolated before and after Al ablation failed to demonstrate any changes in the response properties of neurons in Field P attributable to the ablation. Nonmonotonic response profiles, first spike latency, variability in latency, threshold and maximal discharge rates of the units to acoustic stimuli were not significantly altered by the AI ablation. These results indicate that the basic response properties of neurons in Field P do not depend on input from the ipsilateral AI. This suggests that these properties are most likely determined by thalamic input or by circuitry within Field P.     

Representation of amplitude modulation in the auditory cortex of the cat. I. The anterior auditory field (AAF)

The ability of cortical neurons to follow amplitude modulation (AM) of tones was examined in the anterior auditory cortical field (AAF) of anesthetized cats using multiple-unit recording techniques. Sinusoidal and rectangular modulations (100%) of a monaural carrier tone at the characteristic frequency of each location were presented to study the degree of response synchronization and changes in firing rate as a function of the modulation frequency. All investigated locations were tuned to a 'best modulation frequency' (BMF) as determined by synchronization measures. Almost all locations (94%) were tuned to a BMF as determined by spike rate. Maximal binaural-interaction strength was observed for modulation frequencies close to the BMF of neurons. For sinusoidal AM, a correlation (r = 0.63, P less than 0.01) between BMF and CF of neurons in AAF could be demonstrated for the synchronization of the response.     

Desynchronisation of auditory steady-state responses related to changes in interaural phase differences: an objective measure of binaural hearing

Objective: Binaural processing can be measured objectively as a desynchronisation of phase-locked neural activity to changes in interaural phase differences (IPDs). This was reported in a magnetoencephalography study for 40?Hz amplitude modulated tones. The goal of this study was to measure this desynchronisation using electroencephalography and explore the outcomes for different modulation frequencies. Design: Auditory steady-state responses (ASSRs) were recorded to pure tones, amplitude modulated at 20, 40 or 80?Hz. IPDs switched between 0 and 180° at fixed time intervals. Study sample: Sixteen young listeners with bilateral normal hearing thresholds (≤25?dB HL at 125–8000?Hz) participated in this study. Results: Significant ASSR phase desynchronisations to IPD changes were detected in 14 out of 16 participants for 40?Hz and in 8, respectively 9, out of 13 participants for 20 and 80?Hz modulators. Desynchronisation and restoration of ASSR phase took place significantly faster for 80?Hz than for 40 and 20?Hz. Conclusions: ASSR desynchronisation to IPD changes was successfully recorded using electroencephalography. It was feasible for 20, 40 and 80?Hz modulators and could be an objective tool to assess processing of changes in binaural information.     

Interpretation of brainstem auditory evoked potentials: results from intracranial recordings in humans

The results of recording intracranially from the auditory nerve, lower brainstem nuclei, and the inferior colliculus in more than 40 patients operated upon for hemifacial spasm and trigeminal neuralgia are presented. Recordings from the auditory nerve have shown that the auditory nerve is the neural generator of the first two peaks in the human ABR. Recordings from the entrance of the eighth nerve into the brainstem and locations close to that reveal potentials; the latencies of the peaks in these potentials match those of peaks III and IV. These peaks are therefore assumed to have their source in second-and third-order neurons of the ascending auditory pathway. Recordings from the inferior colliculus show a surface-positive deflection followed by a slow negative wave usually with several undulations. The latency of the positive peak matches that of wave V of the scalp-recorded ABR. It is assumed that the neural generator of this component of the potential recorded from the inferior colliculus is the lateral lemniscus and that the slow, surface-negative potential originates in the inferior colliculus. The latency of this slow potential is too long to explain that nucleus as the neural generator of peak V, as was assumed previously.     

Origin of the binaural interaction component in wave P4 of the short-latency auditory evoked potentials in the cat: evaluation of serial depth recordings from the brainstem

There is no general agreement on the origin of the binaural interaction (BI) component in auditory brainstem responses (ABRs). To study this issue the ABRs to monaural and binaural clicks with various interaural time differences (ITDs) were simultaneously recorded from the vertex and from a recording electrode aiming at the superior olive (SO) in cats. Electrode path was along the fibers of the lateral lemniscus (LL). Binaural difference potentials (BDPs), which were computed by subtracting the sum of the two monaural responses from the binaural response, were obtained at systematic depths and across a range of ITD values. It was observed that only a specific BDP deflection recorded at the level at which lemniscal fibers terminate in the nuclei of LL coincided in time with the most prominent BDP in the cat's vertex-recorded ABRs, the BDP in their wave P4. As ITD was increased, the latency shifts and amplitude decrements of the scalp-recorded far-field BDP wave exactly followed those recorded at this lemniscal near-field BDP locus. The data support our hypothesis that the BI component in wave P4 results from a binaural reduction in dischargings of axons ascending in the LL, with this reduction due to contralateral inhibition of the discharge activity of the inhibitory-excitatory units in the lateral nucleus of the SO. Furthermore, at the level of the SO, the BDP in the responses to contra-leading binaural clicks always had larger magnitudes than those evoked by ipsi-leading ones. This bilateral asymmetry is consistent with the view that the BDP in scalp-recorded ABRs is related to the function of sound lateralization.     

Discharge patterns of cat primary auditory fibers with electrical stimulation of the cochlea

Intact and destroyed cat cochleae were electrically stimulated through round window electrodes. Intact cochleae provided information about fiber properties with acoustic stimuli. With sinusoidal currents thresholds for synchronization were 4–68 μA rms. Thresholds were independent of the fiber's characteristic frequencies and thus of their places of origin in the intact cochleae. This shows large current spread. Phase-locking of the responses to electric stimulation was much stronger than it was to acoustic stimulation. Destroyed cochleae had no spontaneous activity and showed even stronger phase-locking. Thresholds obtained using 0.2 ms per phase biphasic pulse stimuli were 60–350 μA_pp. Action potentials were found to be released with as little as 0.3 ms latency. The neuronal responses to any electric stimulus differed considerably from the responses to corresponding acoustic stimuli. Vestibular fibers were easily activated by electric stimulation.     

Representation of amplitude modulation in the auditory cortex of the cat. II. Comparison between cortical fields

The responses of neuronal clusters to amplitude-modulated tones were studied in five auditory cortical fields of the anesthetized cat: the primary auditory field (AI), second auditory field (AII), anterior auditory field (AAF), posterior auditory field (PAF) and the ventro-posterior auditory field (VPAF). Modulation transfer functions (MTFs) for amplitude-modulated tones were obtained at 172 cortical locations. MTFs were constructed by measuring firing rate (rate-MTFs) and response synchronization (synchronization-MTFs) to sinusoidal and rectangular waveform modulation of CF-tones. The MTFs were characterized by their 'best-modulation frequency' (BMF) and a measure of their quality of 'sharpness' (Q2dB). These characteristics were compared for the five fields. Rate and synchronization MTFs for sinusoidal and rectangular modulation produced similar estimates of BMF and Q2dB. Comparison of averaged BMFs between the cortical fields revealed relatively high BMFs in AAF (mean: 31.1 Hz for synchronization to sinusoidal AM) and moderately high BMFs in AI (14.2 Hz) whereas BMFs encountered in AII, VPAF and PAF were generally low (7.0, 5.2, and 6.8 Hz). The MTFs were relatively broadly tuned (low Q2dB) in AAF and sharper in a low modulation group containing AII, PAF and VPAF. The ventro-posterior field was the most sensitive to changes in the modulation waveform. We conclude that there are significant differences between auditory cortical fields with respect to their temporal response characteristics and that the assessment of these response characteristics reveals important aspects of the functional significance of auditory cortical fields for the coding and representation of complex sounds.     

Spatial sensitivity of neurons in the anterior, posterior, and primary fields of cat auditory cortex

We assessed the spatial-tuning properties of units in the cat's anterior auditory field (AAF) and compared them with those observed previously in the primary (A1) and posterior auditory fields (PAF). Multi-channel, silicon-substrate probes were used to record single- and multi-unit activity from the right hemispheres of alpha-chloralose-anesthetized cats. Spatial tuning was assessed using broadband noise bursts that varied in azimuth or elevation. Response latencies were slightly, though significantly, shorter in AAF than A1, and considerably shorter in both of those fields than in PAF. Compared to PAF, spike counts and latencies were more poorly modulated by changes in stimulus location in AAF and A1, particularly at higher sound pressure levels. Moreover, units in AAF and A1 demonstrated poorer level tolerance than units in PAF with spike rates modulated as much by changes in stimulus intensity as changes in stimulus location. Finally, spike-pattern-recognition analyses indicated that units in AAF transmitted less spatial information, on average, than did units in PAF-an observation consistent with recent evidence that PAF is necessary for sound-localization behavior, whereas AAF is not.     

Temporal envelope processing in the human auditory cortex: response and interconnections of auditory cortical areas

Temporal envelope processing in the human auditory cortex has an important role in language analysis. In this paper, depth recordings of local field potentials in response to amplitude modulated white noises were used to design maps of activation in primary, secondary and associative auditory areas and to study the propagation of the cortical activity between them. The comparison of activations between auditory areas was based on a signal-to-noise ratio associated with the response to amplitude modulation (AM). The functional connectivity between cortical areas was quantified by the directed coherence (DCOH) applied to auditory evoked potentials. This study shows the following reproducible results on twenty subjects: (1) the primary auditory cortex (PAC), the secondary cortices (secondary auditory cortex (SAC) and planum temporale (PT)), the insular gyrus, the Brodmann area (BA) 22 and the posterior part of T1 gyrus (T1Post) respond to AM in both hemispheres. (2) A stronger response to AM was observed in SAC and T1Post of the left hemisphere independent of the modulation frequency (MF), and in the left BA22 for MFs 8 and 16Hz, compared to those in the right. (3) The activation and propagation features emphasized at least four different types of temporal processing. (4) A sequential activation of PAC, SAC and BA22 areas was clearly visible at all MFs, while other auditory areas may be more involved in parallel processing upon a stream originating from primary auditory area, which thus acts as a distribution hub. These results suggest that different psychological information is carried by the temporal envelope of sounds relative to the rate of amplitude modulation.     

The effect of brainstem lesions on brainstem auditory evoked potentials in the cat

Brainstem auditory evoked potentials (BAEPs) were recorded before and after cuts were made in either the midline trapezoid body (TB), the lateral lemniscus (LL), or the combined dorsal and intermediate acoustic striae (DAS/IAS) in 23 anesthetized cats. Monaural and binaural rarefaction clicks were presented at a rate of 10 per s, and the potentials recorded from a vertex electrode referenced to either earbar or to the neck. The potentials were filtered so that fast and slow components could be examined separately and special efforts were exerted to obtain stable conditions so that small changes in waveforms could be significant. Lesions of the DAS/IAS produced negligible changes in either the fast or slow waves. Lesions of the midline TB reduced the amplitudes of peaks P3 through P5, while greatly reducing the amplitude of the slow wave. Complete lesions of the LL always reduced the amplitude of the slow wave. Lesions of the ventral part of the LL were more likely to reduce the amplitude of P4-P5. Our interpretations of these lesion experiments are based on the idea that individual fast peaks of the BAEP represent compound action potentials of fiber pathways. According to this view, only synchronized activity generated in populations of neurons that are both favorably oriented in space and significant in number, will contribute to the fast peak.     

The representation of peripheral neural activity in the middle-latency evoked field of primary auditory cortex in humans(1)

Short sweeps with increasing instantaneous frequency (up-chirps) designed to compensate for the propagation delay along the human cochlea enhance the magnitude of wave V of the auditory brainstem responses, while time reversed sweeps (down-chirps) reduce the magnitude of wave V [Dau, T., Wegner, O., Mellert, V., Kollmeier, B., J. Acoust. Soc. Am. 107 (2000) 1530-1540]. This effect is due to synchronisation of frequency channels along the basilar membrane and it indicates that cochlear phase delays are preserved up to the input of the inferior colliculus. The present magnetoencephalography study was designed to investigate the influence of peripheral synchronisation on the activation in primary auditory cortex. Spatio-temporal source analysis of middle-latency auditory evoked fields (MAEFs) elicited by clicks and up- and down-chirps showed that up-chirps elicited significantly larger MAEF responses compared to clicks or down-chirps. Both N19m-P30m magnitude and its latency are influenced by peripheral cross-channel phase effects. Furthermore, deconvolution of the empirical source waveforms with spike probability functions simulated with a cochlear model indicated that the source waves for all stimulus conditions could be explained with the same unit-response function, i.e. a far field recorded cortical response of a very small cell assembly along the medio-lateral axis of Heschl's gyrus that receives input from a small number of excitatory fibres. The conclusion is that (i) phase delays between channels in the auditory pathway are preserved up to primary auditory cortex, and (ii) MAEFs can be described by a convolution of a unit-response function with the summary neural activity pattern of the auditory nerve.     

The input-output function of the slow auditory evoked potential in contralateral,ipsilateral, and vertex recordings

Summary In the present paper the input-output functions of the slow acoustically evoked potential are determined under the following conditions: vertex-, ipsi-lateral and contra-lateral pick-up. In all three modes of pick-up we got the input-output function of the high stimulus repetition rate;—this means: for the adapted stage of the system as well as that for the small repetition rate, the non-adapted stage. In all three modes of pick-up we found a different input-output-function and a difference between the adapted and the non-adapted stage. The simultaneous registration is more advisable than the successive one. We determined the normal characteristic curves of 10 adults in order to compare them with patients. The vertex-pick-up seems to be the best one for determining the threshold, whereas the contralateral pick-up seems to give more information about the pathological function of the acoustic system.

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Zusammenfassung Die vorliegende Arbeit stellt für den klinischen Gebrauch verwertbare Kennlinien des langsamen akustisch evozierten Potentials auf, und zwar für die folgenden 3 Ableitungsorte: am Vertex, an der ipsilateralen und an der kontralateralen Schläfe. Für diese 3 Ableitungsorte wurde die Kennlinie sowohl bei hoher als auch bei niedriger Reizfolgefrequenz untersucht. An allen 3 Stellen ergaben sich dabei voneinander unterschiedliche Kennlinien; an jedem Ableitort unterscheidet sich die adaptierte Kennlinie (d. h. bei hoher Reizfolgefrequenz) von der nicht-adaptierten (geringe Reizfolgefrequenz), ist aber signifikant größer und erscheint schon bei geringerer Reizintensität bei kontralateraler Ableitung. Die Ergebnisse bei simultaner (alle 3 Ableitungsorte gleichzeitig) und successiver (alle 3 Ableitorte hintereinander) werden verglichen. Anhand der Kennlinien von 10 normalhörenden Versuchspersonen werden die zweier Patienten mit Innenohrstörungen gewertet. Die 3-kanalige, simultane Ableitung ergibt mehr Sicherheit und eine erweiterte Information.

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Supported by the Fonds zur Förderung der wissenschaftlichen Forschung (CAT-Computer Volkwagen-Foundation).     

Effects of an acute acoustic trauma on the representation of a voice onset time continuum in cat primary auditory cortex

Here we show that hearing loss associated with an impairment of speech recognition causes a decrease in neural temporal resolution. In order to assess central auditory system changes in temporal resolution, we investigated the effect of an acute hearing loss on the representation of a voice onset time (VOT) and gap-duration continuum in primary auditory cortex (AI) of the ketamine-anesthetized cat. Multiple single-unit activity related to the presentation of a /ba/-/pa/ continuum--in which VOT was varied in 5-ms step from 0 to 70 ms-- was recorded from the same sites before and after an acoustic trauma using two 8-electrode arrays. We also obtained data for gaps, of duration equal to the VOT, embedded in noise 5 ms after the onset. We specifically analyzed the maximum firing rate (FRmax), related to the presentation of the vowel or trailing noise burst, as a function of VOT and gap duration. The changes in FRmax for /ba/-/pa/ continuum as a function of VOT match the psychometric function for categorical perception of /ba/-/pa/ modeled by a sigmoid function. An acoustic trauma made the sigmoid fitting functions shallower, and shifted them toward higher values of VOT. The less steep fitting function may be a neural correlate of an impaired psychoacoustic temporal resolution, because the ambiguity between /ba/ and /pa/ should consequently be increased. The present study is the first one in showing an impairment of the temporal resolution of neurons in AI caused by an acute acoustic trauma.     

Rate fluctuations and fractional power-law noise recorded from cells in the lower auditory pathway of the cat

The noise properties of the sequence of action potentials recorded from adult-cat auditory nerve fibers and lateral superior olivary units have been investigated under various stimulus conditions. Large fluctuations exhibited by the spike rate, and spike clusters evident in the pulse-number distribution, both indicate an unusual underlying sequence of neural events. We present results demonstrating that (i) the firing rate calculated with different averaging times can exhibit self-similar behavior; (ii) the pulse-number distribution remains irregular even for large numbers of samples; (iii) the spike-number variance-to-mean ratio increases with the counting time T in fractional power-law fashion for sufficiently large T; and (iv) the exponent in the power law generally depends on the stimulus level. The results obtained in our laboratories support the notion that all auditory-nerve and LSO units exhibit fractal neural firing patterns, as indicated earlier by Teich (IEEE Trans. Biomed. Eng. 36, 150-160, 1989).