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Where is 'where' in the human auditory cortex?

We examine the functional characteristics of auditory cortical areas that are sensitive to spatial cues in the human brain, and determine whether they can be dissociated from parietal lobe mechanisms. Three positron emission tomography (PET) experiments were conducted using a speaker array permitting quasi free-field sound presentation within the scanner. Posterior auditory cortex responded to sounds that varied in their spatial distribution, but only when multiple complex stimuli were presented simultaneously, implicating this cortical system in disambiguation of overlapping auditory sources. We also found that the right inferior parietal cortex is specifically recruited in localization tasks, and that its activity predicts behavioral performance, consistent with its involvement in sensorimotor integration and spatial transformation. These findings clarify the functional roles of posterior auditory and parietal cortices, and help to reconcile competing models of auditory cortical organization.

Acoustic Stimulation↗

Distributed representation of spectral and temporal information in rat primary auditory cortex.

Modulations of amplitude and frequency are common features of natural sounds, and are prominent in behaviorally important communication sounds. The mammalian auditory cortex is known to contain representations of these important stimulus parameters. This study describes the distributed representations of tone frequency and modulation rate in the rat primary auditory cortex (A1). Detailed maps of auditory cortex responses to single tones and tone trains were constructed from recordings from 50-60 microelectrode penetrations introduced into each hemisphere. Recorded data demonstrated that the cortex uses a distributed coding strategy to represent both spectral and temporal information in the rat, as in other species. Just as spectral information is encoded in the firing patterns of neurons tuned to different frequencies, temporal information appears to be encoded using a set of filters covering a range of behaviorally important repetition rates. Although the average A1 repetition rate transfer function (RRTF) was low-pass with a sharp drop-off in evoked spikes per tone above 9 pulses per second (pps), individual RRTFs exhibited significant structure between 4 and 10 pps, including substantial facilitation or depression to tones presented at specific rates. No organized topography of these temporal filters could be determined.

Acoustic Stimulation↗

Single-unit activity in the auditory cortex of monkeys actively localizing sound sources: spatial tuning and behavioral dependency.

Single-unit recordings were made from the auditory cortex of unanesthetized rhesus monkeys which were trained to perform a second localization task. Recordings were made from 196 units in 4 animals. Five sound sources were located at 0 degrees (midline) and on either side at azimuths of 37.5 degrees and 75 degrees. Almost most units responded to each of the 5 sources, 49% of the units had peak firing rates for the source on the contralateral side at 75% azimuth. Another 26% of the units had peak firing rates at the 37.5 degrees contralateral location, while only 11% had peak rates for the ipsilateral locations. In order to determine whether the behavior of actively locating a sound source affected units in auditory cortex, response rates compared under two behavioral conditions: one which required the detection of a sound regardless of location and another condition which required identification of a sound's location. of the 196 units, 16 had different response rates for the two conditions, with 15 of the 16 units having higher evoked rates in the localization task. For the 16 units, the difference in firing rate was typically observed for a single speaker location. No correlation could be determined between a unit's location within the subdivisions of auditory cortex and its spatial tuning response properties or its dependency upon behavioral condition.

Animals↗

Cross-correlation and joint spectro-temporal receptive field properties in auditory cortex.

Recordings were made from the right primary auditory cortex in 17 adult cats using two eight-electrode arrays. We recorded the neural activity under spontaneous firing conditions and during random, multi-frequency stimulation, at 65 dB SPL, from the same units. Multiple single-unit (MSU) recordings (281) were stationary through 900 s of silence and during 900 s of stimulation. The cross-correlograms of 545 MSU pairs with peak lag times within 10 ms from zero lag time were analyzed. Stimulation reduced the correlation in background activity, and as a result, the signal-to-noise ratio of correlated activity in response to the stimulus was enhanced. Reconstructed spectro-temporal receptive fields (STRFs) for coincident spikes showed larger STRF overlaps, suggesting that coincident neural activity serves to sharpen the resolution in the spectro-temporal domain. The cross-correlation for spikes contributing to the STRF depended much stronger on the STRF overlap than the cross-correlation during either silence or for spikes that did not contribute to the STRF (OUT-STRF). Compared with that for firings during silence, the cross-correlation for the OUT-STRF spikes was much reduced despite the unchanged firing rate. This suggests that stimulation breaks up the large neural assembly that exists during long periods of silence into a stimulus related one and maybe several others. As a result, the OUT-STRF spikes of the unit pairs, now likely distributed across several assemblies, are less correlated than during long periods of silence. Thus the ongoing network activity is significantly different from that during stimulation and changes afterng arousal during stimulation.

Acoustic Stimulation↗

Neuronal sensitivity to interaural time differences in the sound envelope in the auditory cortex of the pallid bat.

Interaural time differences in the envelope of a sound (envelope ITDs) can potentially provide spatial information at high frequencies where interaural phase differences (IPDs) are not available. Interaural intensity differences (IIDs) also provide important spatial information at high frequencies. Both IIDs and envelope ITDs can influence spatial perception at high frequencies, but behavioral and physiological studies suggest that IIDs dominate perception. This study examines envelope ITD sensitivity in the auditory cortex of the pallid bat, a species that uses passive sound localization at the low end of its audible range to find prey. Its auditory system is entirely 'high-frequency' in that phase-locking does not occur at the low end of its audible range. If the bat uses ITDs, they must be derived from the envelope of the signal. A previous study of envelope ITD sensitivity in its inferior colliculus (IC) reported that neurons are sensitive to the small +/-70 micros range of available ITDs. This study extends these findings to the cortical level to assess the transformation of ITD sensitivity and the binaural response properties that underlie this sensitivity. Two measures of sensitivity were used. The dynamic ITD range measures the range of ITDs over which the maximum response of a neuron decreases by 80%. When presented with square-wave amplitude-modulated tones statically delayed in arrival time, the average dynamic ITD range in the IC is 304 micros, but dropped to 175 micros in auditory cortex. IC neurons average a 38% change in maximum response over the relevant ITD range, while cortical neurons average a 67% change. Also measured were time-intensity trading ratios, which index the extent to which a change in IID can cause a shift the dynamic ITD range. Average trading ratios are approximately the same in the IC and auditory cortex (17.9 micros/dB vs. 16.7 micros/dB, respectively). Binaural interactions changed from the IC to auditory cortex. In IC, ITD sensitivity is an inhibitory, subtractive process in which ITDs reduce the response evoked by contralateral monaural stimulation. In the auditory cortex, both binaural inhibition and facilitation occur. In the majority of cortical neurons, IID and ITD functions were remarkably similar in shape, having stepped, step-peaked or peaked functions. The binaural interactions (inhibition and/or facilitation) evoked by ITDs and IIDs were also typically similar. These results suggest that IIDs and envelope ITDs are having similar effects on output of the same binaural comparator system.

Acoustic Stimulation↗

Sensitization induced receptive field plasticity in the auditory cortex is independent of CS-modality.

Sensitization training with an auditory stimulus produces a general increase in response magnitude across the entire receptive field (RF) of neurons in the primary auditory cortex of the guinea pig (Bakin, J.S. and Weinberger, N.M., Brain Res., 536 (1990) 271-286). To determine if this effect reflects an auditory system-specific process or is caused by a process independent of the training stimulus modality, RFs in primary auditory cortex were characterized before and immediately after adult guinea pigs were given sensitization training with either an auditory or a visual training stimulus. General increases in auditory response magnitude across the RF were observed in 7 out of 7 auditory sensitization cases and 4 out of 5 visual sensitization cases. There were no statistical differences between the effects of auditory and visual sensitization training. These findings indicate that the general increases observed following sensitization training are the result of processes independent of CS modality, in contrast to the highly specific RF modifications that are caused by classical conditioning. The findings suggest that the 2 forms of RF plasticity, CS-specific re-tuning due to associative conditioning and polymodal general increases in gain due to non-associative sensitization, may reflect neural mechanisms involved in selective attention and vigilance, respectively.

Acoustic Stimulation↗

Subject's own speech reduces reactivity of the human auditory cortex.

Previous studies on monkeys have shown that uttering-related cortical areas exert an inhibitory effect on the auditory cortex, and cerebral blood-flow analyses on humans have revealed modulation of the activity of the auditory cortex during own speech. To study this modulation on a millisecond time scale, we recorded neuromagnetic evoked responses to short 1-kHz tones while the subjects were reading silently and aloud. The 100-ms response (M100) of the auditory cortex was delayed by 10-21 ms and its amplitude was dampened by 44-71% during reading aloud compared with reading silently. This effect was more prominent in responses to ipsilateral than contralateral tones, possibly due to a sum effect of diminished ipsilateral input to the cortex and decreased transcallosal excitation.

Acoustic Stimulation↗

Early unilateral auditory deprivation increases 2-deoxyglucose uptake in contralateral auditory cortex of juvenile Mongolian gerbils.

The effects of early onset, unilateral conductive hearing loss on tone-induced 2-deoxyglucose (2-DG) uptake in the auditory cortex of juvenile Mongolian gerbils (Meriones unguiculatus) were studied. Atresia of the left ear canal was induced at postnatal day 9 (P9) to achieve reversible auditory deprivation prior to onset of hearing (around P12). Atresia either persisted (ATR, n=4) or the canal was opened 15 min before the 2-DG experiments (RE, n=4) at P27. Control animals were either non-deprived (CON, n=4), or their left ears were plugged acutely (PAX, n=4). In PAX, 2-DG uptake in primary auditory cortex (AI) and anterior auditory field (AAF) was lower in right than in left AI and AAF. In contrast, in ATR and RE, uptake was significantly higher on the right side contralateral to the atresia. Hence, atresia during early development leads to plastic changes resulting in an interhemispheric imbalance of functional metabolism in favor of the auditory cortex contralateral to the manipulated ear. Distances between tone-induced 2-DG labeling in AI and AAF were increased in PAX, but smaller in ATR in the right compared to the left hemisphere, suggesting effects of atresia also on spatial relations in cortical tonotopic maps.

Acoustic Stimulation↗

Local landmark-based mapping of human auditory cortex.

Mammalian sensory cortex is functionally partitioned into cortical fields that are specialized for different processing operations. In theory, averaging functional and anatomical images across subjects can reveal both the average anatomy and the mean functional organization of sensory regions. However, this averaging process must overcome at least two obstacles: (1) the relative locations and sizes of cortical sensory areas vary in different subjects so that across-subject averaging introduces spatial smearing; (2) the relative locations and sizes of cortical areas vary between hemispheres, making it difficult to compare activations between hemispheres or to combine activations across hemispheres. These difficulties are particularly acute for small cortical regions such as auditory cortex. In whole-brain averaging procedures, considerable intersubject variance in the location and orientation of auditory cortex is introduced by variance of the size and shape of structures outside auditory cortex. Here, we compared these global methods with local landmark-based methods (LLMs) that use warping based on local anatomical landmarks. In comparison to maps made with global methods, LLMs produced anatomical maps of auditory cortex with clearer gyral and sulcal structure, and produce functional maps with improved resolution. These results suggest that LLMs have significant advantages over global mapping procedures in studying the details of auditory cortex organization.

Adult↗

Changes in the acoustically evoked activity in the inferior colliculus of the rat after functional ablation of the auditory cortex.

The role of the cortico-tectal pathways in the processing of auditory signals was investigated by recording the click-evoked responses and extracellular multiple unit activity in the inferior colliculus (IC) after functional ablation of the auditory cortex (AC) by local intracortical application of a sodium channel blocker, tetrodotoxin (TTX). Click-evoked IC responses (IC-ER) and multiple unit activity in response to tone bursts were recorded with implanted electrodes in the IC of rats lightly anaesthetized with xylazine. Neural activity was recorded before and after the application of TTX into the ipsilateral auditory cortex (AC) through three implanted cannulas in a total dose of 30 ng. The functional status of the AC was monitored by recording click-evoked middle latency responses from a ball electrode implanted on the AC. During inactivation of the AC, IC-ER amplitudes were either increased (48 % of the cases), decreased (32 % of the cases) or not evidently changed (20 % of the cases). Corresponding effects were observed in the firing rate of IC neurons. Functional ablation of the AC also resulted in a significant prolongation of the latencies of individual waves of the IC-ER. However, the discharge pattern of the multiple unit responses, response thresholds and tuning were not altered during AC inactivation. IC neural activity recovered within several hours, and maximally during 2 days. The results reveal principles of the interaction of cortico-tectal pathways with IC neuronal activity.

Acoustic Stimulation↗

Intensity-dependent activation of the primary auditory cortex in functional magnetic resonance imaging.

PURPOSE: The purpose of this study was to investigate the activation patterns of the primary auditory cortex in response to varying intensities of pure tone stimuli. METHOD: A 1,000-Hz pure tone stimulus was delivered monaurally to the right ear of 12 normal-hearing right-handed volunteers in 20-second on-off cycles. Stimuli were applied at 20 and 50 dB hearing level (HL) above threshold in 12 subjects and at 0, 20, 40, and 50 dB HL above threshold in 6 subjects. Functional magnetic resonance imaging (fMRI) data were obtained using a 1.5-T scanner and echoplanar imaging. Activated pixels were identified in the transverse temporal gyrus (TTG) of both hemispheres in response to pure tone stimuli at each intensity level using cross-correlation analysis (0.6; P < 0.0001). RESULTS: Of the 24 right and left TTGs imaged (n = 12), activation to pure tone stimuli at 20 and 50 dB HL above threshold was seen in 46% and 79% of TTGs, respectively, with bilateral hemispheric activation in 27% and 64% of subjects, respectively. The mean numbers of activated voxels were 4.0 and 13.0, respectively. Of the 12 right and left TTGs imaged at 0, 20, 40, and 50 dB HL above threshold, activation was seen in 33%, 42%, 58%, and 75% of TTGs, respectively. The mean numbers of activated voxels were 5.8, 3.2, 9.8, and 15.3, respectively. There was a nonsignificant trend toward contralateral (left) dominant TTG activation with increased tone intensity. CONCLUSION: Our results show an increased likelihood of TTG activation, increased TTG activation volume, and increased bilateral hemisphere TTG activation with increasing pure tone intensity. Our results suggest that the primary auditory cortex reflects or is directly involved in the central processing of sound intensity and that varying the intensity of even simple stimuli can alter the patterns of fMRI activation in auditory cortex.

Acoustic Stimulation↗

Primary auditory cortex in the ferret (Mustela putorius): neural response properties and topographic organization.

Microelectrode recording studies were made of the crown of the ectosylvian auditory cortex of barbiturate-anesthetized ferrets, using calibrated, sealed acoustic stimulus delivery systems. We confirmed our previous finding using free-field stimuli that this region of the ferret's cerebral cortex contains a tonotopically organized field in which neurons are briskly excited by the onset of tonal stimuli. The vast majority of neurons in this field were narrowly tuned to tone pulse frequency, with Q factors comparable to those described for cortical cells in other species. The distribution of minimum tone thresholds across the frequency representation of this field paralleled the behavioral audiogram in the same species. The majority of neurons received input from both ears, and the natures of the influences exerted by tonal stimuli at the two ears were similar in form to those described for other carnivores. The various binaural cell types had characteristic frequencies that spanned the entire tonal spectrum represented in the cortex. Preliminary mapping studies revealed that there may be a topographic segregation of cells according to their binaural interactions. The basic properties of cells in this region of the ferret's cerebrum are similar to those previously described for the cat's primary auditory cortex. The data on the binaural properties of these cells, and the spatial distribution of those cells, provide the first evidence in a species other than the cat for segregated binaural representation in the auditory cortex.

Acoustic Stimulation↗

The effect of sequence repeat time on auditory cortex stimulation during phonetic discrimination.

Acoustic noise generated by the MR scanner gradient system during fMRI studies of auditory function is a very significant potential confound. Despite these deleterious effects, fMRI of the auditory cortex has been successful and numerous practitioners have circumvented the problem of acoustic masking noise. In the context of auditory cortex fMRI, the sequence repeat time (TR) has the effect of altering the length of time during which the scanner is quiet. Indeed, the move to whole-brain fMRI makes the problem of acoustic noise more acute and points to the need to examine the role of TR and its influence on the BOLD signal. The aim of this study was to examine the effect of varying the TR time on activation of auditory cortex during presentation and performance of a phonetic discrimination task. The results presented here demonstrate that the influence of sequence repeat time is considerable. For a short repeat time it is likely that the noise from the scanner is a significant mask and hinders accurate task performance. At the other extreme, a repeat time of 9 s is also suboptimal, probably due to attentional effects and lack of concentration and not least because of the longer overall measurement times. The results of this study point to a complicated interplay between psychophysical factors as well as physical parameters; attention, acoustic noise, total duration of the experiment, consideration of the volume of acquisition, and overall difficulty of the task have to be assessed and balanced. For the paradigm used here, the results suggest an optimal TR of around 6 s for a 16-slice acquisition.

Artifacts↗

Spatio-temporal representation of sound intensity in the guinea pig auditory cortex observed by optical recording.

The spatio-temporal representation of sound intensity in the guinea pig auditory cortex was studied by optical recording with the aid of a voltage-sensitive dye. Changes in light intensity due to neural activity induced by sounds at various pressure levels were recorded with a 12 x 12 array of photodiodes. The amplitudes of the responses were displayed as sequential two-dimensional images. The iso-intensity bands revealed by neural activity were orthogonal to the isofrequency bands of tonotopical organization in the anterior field and dorsocaudal field. The frequency-intensity representation through the orthogonal organization varied with time. This mechanism may be adapted to the auditory cortex to sequentially process the three parameters of sound: frequency, intensity, and time. Furthermore, a new field was found in the ventrocaudal region of the auditory cortex. This field showed tonotopicity, but high thresholds.

Acoustic Stimulation↗

Single-unit responses in the auditory cortex of monkeys performing a conditional acousticomotor task.

The general goal of the present study was to assess the response properties to tones of single neurons in the auditory cortex (primary auditory area, A1, and middle lateral auditory belt, ML) of two macaque monkeys while performing an acousticomotor discrimination task requiring a controlled level of attention and motivation. For each neuron, an approximation of the frequency receptive field (FRF) was first established. Second, based on the FRF, sets of paired tone frequencies were defined in which two different tone frequencies had to be associated by the monkey, following a trial and error strategy, to a left or a right key-press with the left arm. After acquisition of the association, the two tones of the pair were presented randomly ("instruction stimulus") and, if the monkey touched the correct key, the stimulus was repeated ("confirmation stimulus") and a reward was delivered. The majority of units (63%) had a FRF formed by multiple peaks, whereas 25% and 12% of units exhibited a simple U-shaped FRF and a "mosaic" FRF, composed of several separated zones of response, respectively. Five principal response patterns were observed: On, Off, On-Off, Sustained, and Inhibition. In relation to the acousticomotor association task, some auditory cortical neurons (33%) exhibited a different response to the same stimulus when presented, in the same trials, as instruction or as confirmation. It was also observed that the response to the same instruction stimulus could differ when comparing correct trials with erroneous trials (wrong motor response). In conclusion, the response properties of auditory cortical neurons in behaving monkeys are strongly dependent on the physical parameters of sounds (frequency, intensity, etc.) as indicated by FRF characteristics, but a substantial influence of the behavioral context and performance may also play an important role.

Acoustic Stimulation↗

[Neuronal populations in the posterior group of thalamic nuclei projecting into the amygdaloid complex and auditory cortex in the cat].

Location of neurons in posterior thalamic nuclei and neighbouring structures of the midbrain regions projecting to the amygdaloid complex and auditory cortex of cat was studied by the method of horseradish peroxidase. The main sources of these brain region projections to amygdaloid complex are peripeduncular , subparafascicular and suprageniculate nuclei and caudal division of the medial geniculate body. The cells of origin of projections to the auditory cortex are located in all medial geniculate nuclei and wide regions of the posterior thalamic group. Neuron pools projecting to the auditory cortex and amygdala exist in medial parts of the posterior thalamic nuclei. The role of posterior thalamic nuclei in transmission of auditory signals to amygdala is discussed.

Amygdala↗

Thalamic and callosal connections of the rat auditory cortex.

This study was designed to assess the relative distributions of two extrinsic afferent fiber systems in the rat auditory cortex as indicated by the patterns of specific lesion-induced degeneration evident in Fink-Heimer preparations. The auditory cortex consists of cytoarchitectural areas 41, 20 and 36. Lesions were made in the medial geniculate body (MGB) or the corpus callosum in some rats, while in other rats, lesions were made in both the MGB and the corpus callosum. Following the thalamic lesions, degenerating terminals occur throughout the auditory region of cortex, principally in layer IV and deep layer III, but also in layer VI and in the superficial part of layer I. With the exception of the band of degeneration in layer I, the density of the thalamic degeneration is uneven, such that patches of increased density of degeneration are separated by regions with few degenerating terminals. Following lesions of the corpus callosum, degenerating callosal terminals are also evident throughout the auditory region of cortex and they occur in deep layer I through layer III, superficial layer V and in layer VI. The density of the degenerating callosal terminals is not uniform throughout most of area 41, to the extent that there are radially-oriented bands of increased density which appear within the continuous callosal projection. Following the double lesions, degenerating terminals throughout the auditory region are distributed homogeneously within all cortical layers with the exception of deep layer V which is relatively free of degeneration. The results indicate that all regions within the rat auditory cortex are subject to both thalamic and callosal influence, although the input is not completely uniform, for the zones in layers IV and VI which have decreased thalamic input appear to have increased callosal input.

Animals↗

Development of Cajal-Retzius cells in the human auditory cortex.

We analysed the differentiation and areal distribution of Cajal-Retzius (C-R) cells in the human auditory cortex using acetylcholinesterase (AChE) technique on specimens ranging between 10 weeks of gestation (w.) and the 3rd postnatal month. AChE-reactive cells appear in the marginal zone of the prospective auditory cortex as early as 10 1/2 weeks of gestation. Analysis of primary and associative auditory cortex in subsequent stages of gestation and during early postnatal life reveals an age-dependent decrease in cell-packing density of C-R cells and an increase in thickness of the marginal zone. Large AChE-reactive cells were readily found in the early postnatal cortex. These and our previous data on the human frontal associative cortex demonstrate the presence of AChE-reactive C-R cells in both primary and associative cortical areas during late fetal and early postnatal life. The postnatal changes in the morphology and distribution of AChE-reactive C-R cells may serve as cellular parameters of the postnatal cortical maturation in man.

Auditory Cortex↗