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Sustained fields of tones and glides reflect tonotopy of the auditory cortex.

Cortical activation in response to two types of auditory stimuli, constant-frequency tones and frequency glides, was studied by measuring the magnetic field outside the head using a whole-head 122-channel magnetometer. Both the magnetic N1m and sustained responses were located in the supratemporal plane of the primary auditory cortex. The sustained responses both to constant-frequency tones and frequency glides reflect tonotopic organization of the auditory cortex both in depth and direction, thus revealing the underlying neuroanatomical structure of the auditory cortex.

Acoustic Stimulation↗

Projections from the auditory cortex to the pontine nuclei in the rabbit.

The pontine projection from the auditory cortex was studied in 24 New Zealand albino rabbits using the method of anterograde transport of HRP-WGA. Microinjections of HRP-WGA (0.03-0.1 microliter) were made in the auditory cortex, which was located by electrophysiological criteria. The auditory cortex was shown to project ipsilaterally to ventral and lateral regions in the caudal pontine nuclei, and to the dorsolateral pontine nuclei in more rostral sections. Labeled terminals were also occasionally seen in the caudal medial pontine nuclei. These results suggest that the auditory cortex can modulate cerebellar input from caudal regions of the pontine nuclei, which project to cerebellar regions shown to be important for classical conditioning.

Animals↗

Role of auditory cortex in the acquisition of differential heart rate conditioning.

Previous findings from our laboratory indicate that lesions of the auditory cortex disrupt the retention of differentially conditioned bradycardiac responses to tonal stimuli in rabbits. In the present experiment, the effect of lesions of the auditory cortex on the acquisition of differential bradycardiac conditioning was examined. The effect of lesions in the auditory cortex were compared to the effect produced by control lesions in the visual cortex. After 7 days of recovery, animals received 7 days of differential Pavlovian bradycardiac conditioning in which one tone (CS+) was paired with the unconditioned stimulus, and another tone (CS-) was never paired with the unconditioned stimulus. All animals demonstrated differential conditioning during the first 3 days of conditioning. On days 4-7, however, auditory cortex lesioned animals did not exhibit significant differential heart rate (HR) conditioning, whereas control animals with lesions in the visual cortex showed no loss of conditioning during this period. The loss of differential conditioning in animals with lesions in the auditory cortex appears to be due to an increase in the magnitude of the response to the CS-. These data support the hypothesis that the auditory cortex serves to inhibit the response to the CS- in differential conditioning of bradycardia to acoustic stimuli, and that the inhibition may be mediated by a descending corticothalamic or corticolimbic pathway.

Animals↗

First-spike timing of auditory-nerve fibers and comparison with auditory cortex.

First-spike timing of auditory-nerve fibers and comparison with auditory cortex. J. Neurophysiol. 78: 2438-2454, 1997. The timing of the first spike of cat auditory-nerve (AN) fibers in response to onsets of characteristic frequency (CF) tone bursts was studied and compared with that of neurons in primary auditory cortex (AI), reported previously. Tones were shaped with cosine-squared rise functions, and rise time and sound pressure level were parametrically varied. Although measurement of first-spike latency of AN fibers was somewhat compromised by effects of spontaneous activity, latency was an invariant and inverse function of the maximum acceleration of peak pressure (i.e., a feature of the 2nd derivative of the stimulus envelope), as previously found in AI, rather than of tone level or rise time. Latency-acceleration functions of all AN fibers were of very similar shape, similar to that observed in AI. As in AI, latency-acceleration functions of different fibers were displaced along the latency axis, reflecting differences in minimum latency, and along the acceleration axis, reflecting differences in sensitivity to acceleration [neuronal transient sensitivity (S)]. S estimates increased with spontaneous rate (SR), but values of high-SR fibers exceeded those in AI. This suggests that S estimates are biased by SR per se, and that unbiased true S values would be less tightly correlated with response properties covarying with SR, such as firing threshold. S estimates varied with CF in a fashion similar to the cat's audiogram and, for low- and medium-SR fibers, matched those for AI neurons. Minimum latency decreased with increasing SR and CF. As in AI, the standard deviation of first-spike timing (SD) in AN was also an inverse function of maximum acceleration of peak pressure. The characteristics of the increase of SD with latency in a given AN fiber/AI neuron and across AN fibers/AI neurons revealed that the precision of first-spike timing to some stimuli can actually be higher in AI than in AN. The data suggest that the basic characteristics of the latency-acceleration functions of transient onset responses seen in cortex are generated at inner hair cell-AN fiber synapses. Implications for signal processing in the auditory system and for first-spike generation and adaptation in AN are discussed.

Acoustic Stimulation↗

SPET monitoring of auditory cortex activation by electric stimulation in a patient with auditory brainstem implant.

Auditory cortex activation following multifrequency acoustic stimulation has been evaluated by means of single photon emission tomography (SPET) in one patient before and after an auditory brainstem implant (ABI). No activation could be observed after acoustic stimulation before ABI. After ABI stimulation in the coronal and axial slices, the activation within the temporal cortex contralateral to the stimulated ear was twice (43.76%) that of normal controls (23.94 +/- 2.74%). This marked difference was not present in other selected cortical auditory areas (homolateral temporal, homolateral and contralateral parietal cortices). The temporal cortex was also examined with six consecutive sagittal slices from 18.75 mm up to 56.25 mm lateral to the midline. A very strong activation (51.20%) compared with that of normal controls (9.94 +/- 7.45%) was detected in the 25.26-mm sagittal slice of the temporal cortex contralateral to the stimulated side. The remaining sagittal slices showed an almost normal post-stimulatory activation. As the 25.26-mm sagittal slice corresponds to the medial part of the auditory temporal cortex, its activation suggests that electrode stimulation is concentrated on the region of the cochlear nucleus in which the neurons that transduce high frequencies are located. SPET can be considered useful, in combination with electric auditory-evoked potentials, to obtain information on ABI placement and function, effectiveness of acoustic stimulation, degree of cortical stimulation and tonotopic spatial distribution of auditory cortex activation.

Adult↗

Cytoarchitectonic parameters of developmental capacity of the human associative auditory cortex during postnatal life.

In order to determine the developmental capacity of the human auditory cortex we studied the 'regressive' cytoarchitectonic events during perinatal and postnatal development: disappearance of fetal elements and cytoarchitectonic reorganization. Studies were done on Nissl-stained serial sections of human temporal cortex in the specimens ranging from 24 weeks of gestation to the 3rd postnatal year. The fetal layers were regularly found in the newborn in the posterior associative auditory cortex. The fetal subplate zone disappeared gradually over the first 3 postnatal months, indicating decline in the growth of the major cortical fibre systems. The fetal types of neurons have been found however also in older specimens in the associative auditory cortex. The auditory cortex also contains in the postnatal period some fetal elements which indicate the presence of prolonged anatomical developmental plasticity.

Auditory Cortex↗

Formation of spike response to sound tones in cat auditory cortex neurons: interaction of excitatory and inhibitory effects.

Responses of the auditory cortical neurons to sound tones were studied extra- and intracellularly in anaesthetized cats. The pattern of response to tone stimuli could most differ in neurons tuned to the same sound frequency and forming a vertical cortical column. Phasic reactions were found in 69% of the neurons studied. Such neurons were encountered in all cortical layers but about 50% of them were localized at a depth of 0.4-1.0 mm, which corresponds to layers III and IV of the auditory cortex. Neurons with phasic reactions were able to respond to a relatively narrow frequency band that demonstrates high discriminative ability of these cells to the frequency analysis of sound signals. Inhibitory processes realized via both forward afferent and recurrent intracortical inhibition mechanisms play particular roles in the formation of phasic reaction of such neurons to different frequency tones. Twenty-six per cent of neurons generated tonic responses to the sound. The majority of such cells (94%) were localized at a depth of 1.0-2.2 mm, which corresponds to cortical layers V and VI. Inhibitory processes exert a much lesser influence on formation of tonic responses in comparison with phasic ones. Neurons of the tonic type, in contrast to phasic neurons, respond to a wider frequency band; their lower ability to discriminate sound frequency is obvious. Parameters of the responses of tonic neurons strictly correlated with the duration and intensity of the acoustic signal. The possibility of some tonic neurons playing an inhibitory role in auditory cortex is discussed [Volkov I. O. et al. (1989) Neurophysiology, Kiev 21, 498-506, 613-620 (in Russian)]. A small portion of the auditory area AI neurons (2%) demonstrated the suppression of background activity during tone stimulation. They were localized mainly in deep cortical layers (V and VI). Intracortical inhibition is supposed to play a dominant role in the formation of this type of response. About 3% of the studied auditory cortex neurons with background activity generated no response to tonic stimuli. Such cells were usually encountered in the superficial auditory cortex layers (I and II).

Acoustic Stimulation↗

Processing of complex sounds in the auditory cortex of cat, monkey, and man.

One of the fundamental features in the organization of sensory cortices which has emerged from 30 years of research in the visual system is the existence of multiple representation of the sensory world in the cerebral cortex. Compared with the visual system much less information exists about the functional specialization of multiple maps in the central auditory system. This is surprising, since an understanding of central auditory representations seems necessary for an understanding of higher auditory processing, including the perception of speech and the perception of auditory space. We have recorded single neuron activity in higher areas of auditory cortex of cats and rhesus monkeys. In cats, activity was recorded in the caudal part of the anterior ectosylvian (AE) cortex (areas AEA and AAF). More than half of the neurons were clearly tuned to the location of a sound source in azimuth and elevation. Frequency-modulated (FM) sounds elicited best responses at fast rates of modulation. By contrast, neurons in the posterior ectosylvian (PE) areas (PAF, VPAF) responded better to slow FM rates. This suggests a possible specialization for the processing of spatial attributes in the AE cortex, and a possible preference for auditory "patterns" in PE. In macaque monkeys, we explored the question of parallel processing in the higher auditory pathways by combining lesion and anatomical tracer techniques with single unit recording. Inactivation of primary auditory cortex (AI) abolished pure-tone responses in the caudomedial area (CM), but not in the rostral area (R). Injections of retrograde fluorescent tracers into R showed strong labeling of the main, ventral nucleus of the medial geniculate (MGv). Both findings suggest the existence of parallel pathways in the auditory cortex, originating at more peripheral sites and possibly specialized for the processing of auditory space vs. auditory patterns. The auditory pattern pathway in Macaque auditory cortex was further explored by using complex stimuli including Macaque-specific communication sounds. Neurons in the lateral belt areas (AL, ML, and CL) respond very selectively to bandpassed noise stimuli, to FM sounds of a certain rate and direction, as well as to certain classes of monkey calls. We are now in the process of exploring higher areas of human auditory cortex by measuring cortical activation with noninvasive functional magnetic resonance imaging (fMRI) while stimulating with complex auditory sounds.

Animals↗

Spatial distribution of responses to simple and complex sounds in the primary auditory cortex.

The basic functional organization of the cat primary auditory cortex is discussed as it is revealed by electrophysiological studies of the distribution of elementary receptive field (RF) parameters. RFs of cortical neurons have been shown to vary considerably from neuron to neuron; additionally, specific RF properties vary independently. Furthermore, some of the RF properties are nonhomogeneously distributed across the auditory cortex and can be interpreted as forming "maps" that represent specific stimulus information in a topographic way. Accordingly, the functional organization of the primary auditory cortex is interpreted as a series of superimposed independent parameter maps. The consequences of such a layout for the spatial and temporal coding of pure tones and speech sounds is illustrated and ramifications for the interpretation of far-field event-related potentials are discussed.

Animals↗

Long-term potentiation of supragranular pyramidal outputs in the rat auditory cortex.

In supragranular layers of the rat auditory cortex, white matter stimulation produces antidromic and transsynaptic field potentials, of which only the latter shows long-term potentiation (LTP) following tetanic stimulation of the white matter. In this study, we investigated the cells responsible for the LTP. The transsynaptic field potentials, excitatory postsynaptic potentials (EPSPs), and orthodromic spikes were blocked by 6-cyano-7-nitroquinoxaline-2,3-dione (10 microM), but not by D-2-amino-5-phosphonovalerate (D-AP5, 50 microM). The latency of EPSPs was constant, while that of transsynaptic field potentials and orthodromic spikes was shortened by the increase in stimulus intensity. Appearance of antidromic field potentials and antidromic spikes at strong stimulus intensities were accompanied by reduction in amplitude of transsynaptic field potentials and elimination of orthodromic spikes, respectively. Morphological identification of neurons showing antidromic spikes by intracellular injection of biocytin revealed that most of them were supragranular pyramidal cells. The effects of tetanic stimulation were studied by intracellular recording in seven neurons showing antidromic spikes, and it was found that only two of them showed LTP of EPSP slope. However, in all of the other eight units showing antidromic spikes and recorded extracellularly, LTP was clearly observed in orthodromic firing probability. The LTP induction in the orthodromic firing probability was blocked by D-AP5. These findings indicate that the LTP in field potentials corresponds to LTP in supragranular pyramidal outputs, and the input-output relationship in neural networks of the adult rat auditory cortex is strongly modulated by LTP.

Animals↗

Development of acetylcholinesterase (AChE) staining in human fetal auditory cortex.

In this study acetylcholinesterase (AChE) staining methods have been used to demonstrate the development of the prospective afferent fibres of auditory cortex in human fetuses ranging between 8 and 28 weeks of gestation. Earliest AChE positive staining was found in fetuses at 20--24 weeks in the neuropil of the marginal zone and throughout subplate layer of the auditory cortex. On the basis of this characteristic AChE staining pattern, the auditory cortex may be delineated from surrounding cortical areas. At 24--26 weeks, during intensive lamination of the cortical plate, AchE-positive reaction appears in the deep part of the cortical plate. In the oldest fetuses (28 weeks) a columnar pattern of vertical, darkly stained zones was seen in the middle third of the cortical plate. We conclude that AChE staining is characteristically distributed within cytoarchitectonic compartments and 'synaptic' layers of the developing auditory cortex. The AChE-positive layers coincide with the laminar pattern of synpatogeneis. Thus, AChE-positive reaction during development may serve as a parameter of cortical afferent (thalamic?) innervation of the auditory cortex. In addition, AChE reactivity may indicate the specific transmitter nature of the afferent fibres in the auditory cortex.

Acetylcholinesterase↗

Local haemodynamic changes associated with neural activity in auditory cortex.

We used an optical technique to study haemodynamic changes associated with acoustically driven activity in auditory cortex of the chinchilla. Such changes are first detectable c. 0.5 s after stimulation, peak at 2-3 s, and decay within a further 3-6 s. This intrinsic signal imaging reveals activity in separate cortical areas, including primary auditory cortex (AI), secondary auditory cortex (AII) and an anterior auditory field (AAF). We have measured the timing of haemodynamics associated with each area, and find that AI has a different time course from AII and AAF; its haemodynamic change recovers more rapidly. We also show that within AI and AII, place specific activity related to acoustic stimulus frequency can be resolved by this optical imaging method. Our results show the close association between blood flow change and the local metabolic demands of neural activity. The data provide information about the potential of other functional imaging methods (e.g. PET, fMRI) which rely on activity related haemodynamic events.

Acoustic Stimulation↗

Layer-specific horizontal propagation of excitation in the auditory cortex.

Optical imaging was conducted in rat auditory cortex slice preparations to study how horizontal excitation propagates in the cerebral cortex. When a horizontal cut was made between supragranular and infragranular layers, electrical stimulation of layer II/III elicited horizontally propagating excitation in supragranular layers with the same propagating velocities as those seen before a cut was made. Electrical stimulation of layer VI or the border between the white matter and layer VI also elicited horizontally propagating excitation in infragranular layers with the same propagating velocities as those seen before a cut was made. These results suggest that the horizontal propagation of excitation in supragranular and infragranular layers can occur independently in the auditory cortex.

Animals↗

Frequency change detection in human auditory cortex.

We offer a model of how human cortex detects changes in the auditory environment. Auditory change detection has recently been the object of intense investigation via the mismatch negativity (MMN). MMN is a preattentive response to sudden changes in stimulation, measured noninvasively in the electroencephalogram (EEG) and the magnetoencephalogram (MEG). It is elicited in the oddball paradigm, where infrequent deviant tones intersperse a series of repetitive standard tones. However, little apart from the participation of tonotopically organized auditory cortex is known about the neural mechanisms underlying change detection and the MMN. In the present study, we investigate how poststimulus inhibition might account for MMN and compare the effects of adaptation with those of lateral inhibition in a model describing tonotopically organized cortex. To test the predictions of our model, we performed MEG and EEG measurements on human subjects and used both small- (<1/3 octave) and large- (>5 octaves) frequency differences between the standard and deviant tones. The experimental results bear out the prediction that MMN is due to both adaptation and lateral inhibition. Finally, we suggest that MMN might serve as a probe of what stimulus features are mapped by human auditory cortex.

Adaptation, Physiological↗

Fast temporal interactions in human auditory cortex.

The temporal resolution of the human primary auditory cortex (AC) was studied using middle-latency evoked fields. Paired sounds with either the same or different spectral characteristics were presented with gaps between the sounds of 1, 4, 8 and 14 ms. Spatio-temporal modelling showed (1) that the response to the second sound was recognizable with gaps of 1 ms and rapidly increased in amplitude with increasing gap durations, (2) an enhanced N40m amplitude at gaps > 4 ms, (3) delayed N19m-P30m latencies when the stimuli were different. The median psychoacoustical thresholds were 1.6 ms for the same stimuli and 2.5 ms for different stimuli, confirming the electrophysiological evidence for rapid pattern-specific temporal processing in human primary auditory cortex.

Acoustic Stimulation↗

Evoked potentials of the auditory cortex of the porpoise, Phocoena phocoena.

Evoked potential (EP) recordings in the auditory cortex of the porpoise, Phocoena phocoena, were used to obtain data characterizing the auditory perception of this dolphin. The frequency threshold curves showed that the lowest EP thresholds were within 120-130 kHz. An additional sensitivity peak was observed between 20 and 30 kHz. The minimal EP threshold to noise burst was 3 X 10(-4) - 10(-3) Pa. The threshold for response to modulations in sound intensity was below 0.5 dB and about 0.1% for frequency modulations. Special attention was paid to the dependence of the auditory cortex EP on the temporal parameters of the acoustic stimuli: sound burst duration, rise time, and repetition rate. The data indicate that the porpoise auditory cortex is adapted to detect ultrasonic, brief, fast rising, and closely spaced sounds like echolocating clicks.

Acoustic Stimulation↗

The relationship between the auditory cortex and the claustrum in the cat.

The relationship between the primary auditory cortex and the claustrum has been re-examined in the cat with axoplasmic flow and axonal degeneration methods. Labelled cells are found in a restricted part of the claustrum after injections of HRP or HRP-WGA in the primary auditory cortex, but they are relatively few in number and are palely stained. The number of labelled cells and their depth of staining are greatest at 72 h (the longest survival time used here), and this survival period an occasional labelled cell is also present in the claustrum of the contralateral hemisphere. No labelled cells are seen after 24 h. After small lesions in the primary auditory cortex, fibre and terminal degeneration are present in the part of the claustrum where labelled cells are seen with axoplasmic flow techniques. It is concluded that there are reciprocal connections between the primary auditory cortex and the claustrum, but the rate of axoplasmic flow is unusually slow.

Animals↗

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.

Acoustic Stimulation↗