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Injury-induced reorganization in adult auditory cortex and its perceptual consequences.

Restricted cochlear lesions in adult animals result in a reorganization of auditory cortex such that the cortical region deprived of its normal input by the lesion is occupied by expanded representations of adjacent cochlear loci, and thus of the frequencies represented at those loci. Analogous injury-induced reorganization is seen in somatosensory, visual and motor cortices of adult animals after restricted peripheral lesions. The occurrence of such reorganization in a wide range of species (including simian primates), and across different sensory systems and forms of peripheral lesion, suggests that it would also occur in humans with similar lesions. Direct evidence in support of this suggestion is provided by a small body of functional imaging evidence in the somatosensory and auditory systems. Although such reorganization does not seem to have a compensatory function, such a profound change in the pattern of cortical activation produced by stimuli exciting peri-lesion parts of the receptor epithelium would be expected to have perceptual consequences. However, there is only limited psychophysical evidence for perceptual effects that might be attributable to injury-induced cortical reorganization, and very little direct evidence for the correlation between the perceptual phenomena and the occurrence of reorganization.

Animals↗

Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex.

Functional magnetic resonance imaging (FMRI) detects focal MRI signal changes in brain tissue that are believed to result from changes in neuronal activity. We describe the dependence of this response in auditory cortex on the rate of presentation of simple speech stimuli. Speech syllables were presented to five normal subjects at rates ranging from 0.17 to 2.5 Hz, while the subjects performed a phoneme discrimination task. Regions studied with FMRI during this task included the lateral aspect of both temporal lobes. All subjects showed bilateral superior temporal lobe MRI signal increases that were coincident with stimulus presentation and performance of the task. The magnitude of this response increased in a monotonic, non-linear manner with increasing stimulus rate. This rate-response relationship was nearly identical in right and left hemispheres. The relationship may reflect metabolic activity integrated over time and subject to non-linear characteristics of neuronal recovery or blood flow regulation. The dependence of response magnitude on stimulation rate supports the hypothesis that the FMRI phenomenon indirectly reflects neuronal metabolic activity. The measures provided here should assist in the design of optimal activation strategies for the human auditory cortex.

Adult↗

Representation of cochlea within primary auditory cortex in the cat.

The representation of sound frequency (and of the cochlear partition) within primary auditory cortex has been investigated with use of microelectrode-mapping techniques in a series of 25 anesthetized cats. Among the results were the following: 1) Within vertical penetrations into AI, best frequency and remarkably constant for successively studied neurons across the active middle and deep cortical layers. 2) There is an orderly representation of frequency (and of represented cochlear place) within AI. Frequency is rerepresented across the mediolateral dimension of the field. On an axis perpendicular to this plane of rerepresentation, best-frequency (represented cochlear place) changes as a simple function of cortical location. 3) Any given frequency band (or sector of the cochlear partition) is represented across a belt of cortex of nearly constant width that runs on a nearly straight axis across AI. 4) There is a disproportionately large cortical surface representation of the highest-frequency octaves (basal cochlea) within AI. 5) The primary and secondary field locations were somewhat variable, when referenced to cortical surface landmarks. 6) Data from long penetrations passing down the rostral bank of the posterior ectosylvian sulcus were consistent with the existence of a vertical unit of organization in AI, akin to cortical columns described in primary visual and somatosensory cortex. 7) Responses to tonal stimuli were encountered in fields dorsocaudal, caudal, ventral, and rostral to AI. There is an orderly representation of the cochlea within the field rostal to AI, with a reversal in best frequencies across its border with AI. 8) Physiological definitions of AI boundaries are consistent with their cytoarchitectonic definition. Some of the implications of these findings are discussed.

Acoustic Stimulation↗

Evidence for reactive magnetic 10-Hz rhythm in the human auditory cortex.

We tested the hypothesis that neurons in the human auditory cortex show spontaneous oscillations around 10 Hz, and that this activity ('tau' rhythm) is affected by auditory input. Cortical activity was recorded with a 122-channel whole-scalp neuromagnetometer from healthy adults while they were presented with monaural 500-ms bursts of white noise. The reactivity of spontaneous oscillations was studied over the whole cortex using the Temporal Spectral Evolution method. Oscillatory 6.5-9.5 Hz activity, with sources in the superior temporal lobes, was transiently suppressed by the sounds in eight out of nine subjects. Our results support the existence of a distinct, reactive auditory rhythm in the human temporal cortex.

Adult↗

Frequency of gamma activity is modulated by motivation in the auditory cortex of cat.

Repetitive acoustic stimuli elicit steady-state response (SSR) in the gamma-band both in humans and in mammals. Our aim was to investigate changes of the spontaneous gamma activity and the SSR in the auditory cortex of cats in the background of an instrumental conditioning situation. Epidural electrodes were chronically implanted above the auditory neocortex. The presentation rate of the clicks varied between 20 and 65/s. Spontaneous EEG and SSR were collected in three behavioral states: in an indifferent environment, in the instrumental cage while the cat was waiting for the light CS, and when she stepped on the pedal and was waiting for the meat reward. Using different repetition rate clicks we determined which stimulus rate elicited the largest SSR in these three situations. In quiet animal the highest SSR appeared at 28-30/s. Before and during the CS the optimal stimulus rate shifted to 32-38/s. The frequency of the spontaneous gamma activity changed in parallel way depending on the situation. We conclude that both the SSR and the spontaneous gamma activity reflect resonant activity of the same neuronal circuit of the auditory cortex, and it is modulated by the motivational state of the animal.

Animals↗

Near-field responses from the round window, inferior colliculus, and auditory cortex of the unanesthetized chinchilla: manipulations of noiseburst level and rate.

Few studies have compared the response properties of near-field potentials from multiple levels of the auditory nervous system of unanesthetized animals. The purpose of this study was to investigate the effects of brief-duration noisebursts on neural responses recorded from electrodes chronically implanted at the round window, inferior colliculus and auditory cortex of chinchillas. Responses were obtained from seven unanesthetized chinchillas to a noiseburst-level and noiseburst-rate series. For the noiseburst-rate series, a 70 dB pSPL noiseburst was varied in rate from 10 to 100 Hz using conventional averaging procedures, and from 100 to 500 Hz using pseudorandom pulse trains called maximum length sequences (MLSs). Response thresholds were similar for the compound action potential (CAP), inferior colliculus potential (ICP) and auditory cortex potential (ACP). With decreasing noiseburst level, there were decreases in the amplitudes and increases in the latencies of the CAP, ICP and ACP. The shapes of the mean normalized amplitude input/output (I/O) functions were similar for the ICP and ACP, while the normalized I/O functions for the first positive peak (P1) and first negative peak (N1) of the CAP differed from each other and from the ICP and ACP. The slopes of the latency/intensity functions were shallowest for the CAP, intermediate for the ICP, and steepest for the ACP. With increasing rate, the latency shift was least for the CAP, intermediate for the ICP and greatest for the ACP. The amplitude of P1 of the CAP varied little with rate. All other potentials showed a pronounced decrease in amplitude at high stimulation rates. Excluding CAP P1, proportional amplitude decrease with rate was greatest for the ACP, intermediate for N1 of the CAP and least for the ICP. Responses were present in most animals at all recording sites, even for the highest rate (500 Hz) used in this study. For all potentials, the MLS procedure allowed the collection of a response at rates well above those where sequential responses would have overlapped using conventional averaging procedures.

Anesthesia↗

Differential frequency conditioning enhances spectral contrast sensitivity of units in auditory cortex (field Al) of the alert Mongolian gerbil.

Differential aversive auditory conditioning in the awake Mongolian gerbil was performed during single- and multi-unit recording in field Al of the primary auditory cortex. Presentations of pure tone stimuli of a given frequency (reinforced conditioned stimulus; CS+) paired with electrocutaneous stimulation (unconditioned stimulus) were combined with several other non-reinforced tone stimuli (non-reinforced conditioned stimulus; CS-). Stimulus presentation during training and testing was optimized for constancy of the probability of occurrence of both the CS+ and the CS- stimulus. The paradigm led to a reorganization of both the spectral and temporal response characteristics of auditory cortical neurons with the following basic results. First, tone-evoked responses of Al neurons recorded after multiple acoustic stimulation under these conditions varied statistically around a mean value (stationarity). Conditioning produced a shift in mean values of evoked responses. The altered tone responses were also stationary (stability of the plastic effects). Second, the frequency-receptive fields (FRFs) of neurons were reorganized in a frequency-specific way such that the CS+ frequency became located in a local minimum of the FRF after training. This resulted from a training-induced increase in the responses to frequencies adjacent to the CS+ frequency in the FRF relative to the CS+ response. The effect can be interpreted as an enhancement of the 'spectral contrast' sensitivity of the unit in the CS+ neighbourhood. Third, apart from this frequency-specific plastic effect, responses to other frequencies also underwent changes during training. The non-frequency-specific changes were not generally predictable but the post-trial responses were stationary. Fourth, the analysis of the long-term behaviour of FRF reorganization revealed the stability of plastic effects under retention training and the gradual re-establishment of the pretrial FRF during extinction training. Fifth, not only the spectral characteristics but also the temporal structure of the tone-evoked responses could be affected by the training. In most cases the training-induced changes measured within the first tens of milliseconds of the response corresponded to the response changes obtained by integration over the total response period. There were some cases, however, in which the direction of the response change varied with time, indicating that excitatory and inhibitory influences on the temporal response pattern were differently affected by training.

Acoustic Stimulation↗

[Magnetic stimulation of the auditory cortex for disabling tinnitus: preliminary results].

OBJECTIVE: Tinnitus - the perception of sound in one or both ears or in the head when no external sound is present - can be disabling and is especially difficult to treat. Repetitive transcranial magnetic stimulation (rTMS) is a noninvasive technique for activating or inactivating specific areas of the cortex. The aim of this study was to assess the feasibility of magnetic neurostimulation of the primary and secondary auditory cortex in the treatment of disabling chronic tinnitus. PATIENTS AND METHODS: Thirteen patients with tinnitus refractory to several conventional treatments underwent transcranial magnetic stimulation guided by functional magnetic resonance imaging (fMRI). We compared two types of stimulation of targets in the auditory cortex, identified by fMRI: 3-second pulses at high frequency (10 Hz) and 20-minute stimulations at a lower frequency (1 Hz). RESULTS: Brief high-frequency pulses of cortical magnetic stimulation (10 Hz) were not effective. On the other hand, prolonged low frequency (1 Hz) stimulation was effective in 62.5% of patients; the effect appeared 48 h after treatment and lasted for approximately 5 days. DISCUSSION: RTMS may be a new noninvasive technique for studying the cortical plasticity associated with the pathophysiologic mechanisms of chronic tinnitus and may lead to new treatment strategies for patients with disabling tinnitus resistant to all treatment.

Adult↗

Processing of complex sounds in the human auditory cortex as revealed by magnetic brain responses.

Processing of simple and complex sounds in the human brain was compared by recording extracranial magnetic mismatch responses (MMNm; the magnetic counterpart of the mismatch negativity, or MMN) to frequency changes in these sounds. Generator sources, modeled as equivalent current dipoles (ECDs), of MMNm responses to a change in one frequency element of complex sounds (a chord and a serial tone pattern) were located in supratemporal auditory cortex, on average, 10 mm medially to the source of an MMNm elicited by an identical frequency change in a simple tone. These results suggest that at least partially different supratemporal neuron populations are involved in processing changes in simple and complex sounds and that sensory-memory representations for these sounds may be located in different fields of the auditory cortex.

Adult↗

Responses of single neurones in cat auditory cortex to time-varying stimuli: frequency-modulated tones of narrow excursion.

In the primary auditory cortex of cats anaesthetized with nitrous oxide, single neurones were examined with respect to their responses to tone bursts and linear modulations of the frequency of an on-going continuous tone. Using FM ramps of 2.0 kHz excursion and varying centre frequency, each of 39 neurones was examined for its preference for the direction of frequency change of a ramp whose centre frequency was varied in and around the neurone's response area. Direction preference was strictly associated with the slopes of the cell's spike count-versus-frequency function over the frequency range covered by the ramp. Preferences for upward- and downward-directed ramps were associated with the low- and high-frequency slopes of the spike count function, respectively. The strength of the cell's direction preference was associated with the relative steepness of the spike count function over the frequency range covered by the ramp. The timing of discharges elicited by the frequency modulations was found to be the sum of the cell's latent period for tone bursts plus the time after ramp onset that the stimulus frequency fell within the neurone's response area. The implications of these data for the processing of narrow and broad frequency-modulated ramps are discussed.

Animals↗

Evoked unit activity in auditory cortex of monkeys performing a selective attention task.

Single-unit responses were recorded from the auditory cortex of rhesus monkeys performing a selective atteintion task which used combined light and sound stimuli. The animals were first trained to push a lever to the left for a noise burst and to the right for a tone burst, and then trained to push left for a left light and right for a right light. Subsequently, one of the four possible light and sound stimulus combinations (Noise + Left Light, Noise + Right Light, Tone + Left Light, Tone + Right Light) was randomly presented on each trial. In blocks of 100 trials only one part of the combined stimulus (either the light or the sound) determined the direction of lever push that would be reinforced. Responses of single units to identical sound stimuli were compared for blocks in which sound was the relevant cue and blocks in which light was the relevant cue. Typically, differences were in response strength without alteration of response pattern. Even the earliest response components (15-20 msec latency) could show changes. Two-thirds of the response comparisons showed differences in strength depending upon whether sound or light was the relevant cue, with about as many responses stronger for light relevant as for sound relevant. Independent of which modality was relevant, unit responses for trials in which both parts of the combined light and sound stimulus indicated the same direction of lever push were generally stronger than unit responses for trials in which the two parts of the combined stimulus signalled opposite directions of lever pushes.

Animals↗

When the auditory cortex turns visual.

We studied visually guided behavior and the visual response properties of single auditory cortex (A1) neurons in neonatally operated hamsters with surgically induced, permanent, ectopic retinal projections to auditory thalamic nuclei and to visual thalamic nuclei which normally receive little direct retinal input. The surgically induced retino-thalamo-cortical pathways can mediate visual guided behaviors whose normal substrate, the pathway from the retina to the primary visual cortex via the primary thalamic visual nucleus, is missing. The visually evoked response properties of A1 neurons resemble in many respects those of neurons in V1 of normal hamsters: many A1 neurons have well-defined visual receptive fields and preferences for orientation or direction of movement. In addition, some visually responsive cells in A1 are bimodal--they also respond to auditory stimuli. The visually responsive neurons in A1 probably account for the capacity of the auditory cortex to mediate visual behavior in 'rewired hamsters'.

Animals↗

Temporal integration in the human auditory cortex as represented by the development of the steady-state magnetic field.

The threshold for detecting amplitude modulation (AM) decreases with increasing duration of the AM sound up to several hundred milliseconds. If the auditory evoked steady-state response (SSR) to AM sound is an electrophysiological correlate of AM processing in the human brain, the development of the SSR should follow this course of temporal integration. Magnetoencephalographic recordings of SSR to 40 Hz AM tone-bursts were compared with responses to non-modulated tone-bursts at inter-stimulus intervals (ISIs) of 3, 1, and 0.5 s. Both types of stimuli elicited a transient gamma-band response (GBR), an N1 wave, and a sustained field (SF) during stimulus presentation. The AM stimulus evoked an additional 40 Hz SSR. The N1 amplitude was strongly reduced with shortened ISI, whereas the amplitudes of SSR, GBR, and SF were little affected by the ISI. Magnetic source-localization procedures estimated the generators of the early GBR, the SSR, and the SF to be anterior and medial to the sources of the N1. The sources of the SSR were in primary auditory cortex and separate from GBR sources. The SSR amplitude increased monotonically over a 200 ms period beginning about 40 ms after stimulus onset. The time course of the SSR phase reliably measured the duration of this transition to the steady state. At stimulus offset the SSR ceased within 50 ms. These results indicate that the primary auditory cortex responds immediately to stimulus changes and integrates stimulus features over a period of about 200 ms.

Acoustic Stimulation↗

Tonotopic organization in auditory cortex of the cat.

Microelectrode mapping techniques were employed in the cat's auditory cortex to relate the best frequencies of a large population of neurons with their spatial loci. Based upon the best-frequency distribution, the auditory region was divided into four complete and orderly tonotopic representations and a surrounding belt of cortex in which the tonotopic organization was more complex. The four auditory fields occupy a crescent-shaped band of tissue which comprises portions of both the exposed gyral surfaces and sulcal banks of the ectosylvian cortex. The anterior auditory field (A) is situated most rostrally upon the anterior ectosylvian gyrus. It extends upon the ventral bank of the suprasylvian sulcus and upon the banks of the anterior ectosylvian sulcus. Adjoining field A caudally is the primary auditory field (AI), which extends across the middle ectosylvian gyrus and portions of both banks of the posterior ectosylvian sulcus. The representations of the highest best frequencies in fields A and AI are contiguous. Caudal and ventral to AI are located the posterior (P) and ventroposterior (VP) auditory fields. They lie mainly upon the caudal bank of the posterior ectosylvian sulcus but also extend upon the rostral bank and upon the posterior ectosylvian gyrus. The low best-frequency representations of fields AI and P are contiguous, whereas the low best-frequency representation of field VP lies near the ventral end of the posterior ectosylvian sulcus. Fields P and VP are joined along their middle and high best-frequency representations. Within each auditory field isofrequency lines defined by the spatial loci of neurons with similar best frequencies are oriented orthogonal to the low-to-high best-frequency gradients.

Animals↗

The alpha 2-adrenergic antagonist idazoxan enhances the frequency selectivity and increases the threshold of auditory cortex neurons.

Idazoxan (IDA), an alpha 2 antagonist of adrenoceptors, has been shown to increase cortical release of norepinephrine (NE) by an action mediated primarily by the alpha 2 autoreceptors located on the NE terminals. In the present experiment, IDA application was used to increase the cortial concentration of NE. Single unit activity (n = 107) was recorded in the rat auditory cortex, and the neurons' frequency receptive fields (FRF) were determined before and after systemic (intraperitoneal or intravenous) or local application of IDA. In the whole population (n = 107) there was a decrease in spontaneous activity and/or evoked activity for 84% of the recordings (90/107 cells). Decreased tone-evoked responses were obtained after systemic injections (n = 39), as well as after local applications (n = 68) of IDA. These effects were not observed after either systemic injections (n = 13) or local applications (n = 9) of saline. The signal-to-noise ratio (the mean evoked responses divided by the spontaneous activity) was slightly decreased after systemic injections and slightly increased after local applications. However, after both systemic and local injections the frequency selectivity of the neuronal responses was increased. For a group of neurons (n = 27), testing the FRF at three intensities indicated that this increased selectivity can be expressed at high or middle range intensity but not at low intensity. For 37 cells, the intensity function was tested at the best frequency before and after IDA application, and the threshold for excitatory responses was determined in 28 cases. An increased threshold was observed in 16 of 28 cases after IDA application. Thus, using a pharmacological procedure to increase the extracellular concentration of NE, the dominant inhibitory effect on the auditory cortex neurons led to an enhancement of the frequency selectivity, but also an increase in the threshold of these neurons.

Acoustic Stimulation↗

Long-term potentiation of Ca2+ signal in the rat auditory cortex.

The Ca2+ signal in supragranular layers of the rat auditory cortex (AC) was studied in slice preparations using rhod-2, a Ca2+ indicator. White matter stimulation elicited an increase in the Ca2+ signal, which was maximal in the image taken 34 ms after stimulation. This peak time was the same as that of the Ca2+ signal in pyramidal neurons injected with rhod-2. The intensity of the Ca2+ signal was proportional to the amplitude of the field potentials in supragranular layers. The Ca2+ signal was inhibited almost completely by 200 microM Ni2+ , but only slightly by 50 microM D-2-amino-5-phosphonovalerate (APV), an NMDA-receptor antagonist. Tetanic stimulation of the white matter or supragranular layers elicited long-term potentiation (LTP) of the Ca2+ signal in AC slices, but the potentiation was not clear in slices of the visual cortex (VC). The induction of LTP of the field potentials in AC slices was blocked by 50 microM APV or 50 microM Ni2+. These results indicate that Ca2+ influx through Ni2+ -sensitive Ca2+ channels in pyramidal neurons is potentiated by tetanic stimulation in parallel with LTP of neural activities and might be important for the induction of LTP in AC slices.

2-Amino-5-phosphonovalerate↗

Encoding of sound-source location and movement: activity of single neurons and interactions between adjacent neurons in the monkey auditory cortex.

1. Neuronal mechanisms for decoding sound azimuth and angular movement were studied by recordings of several single units in parallel in the core areas of the auditory cortex of the macaque monkey. The activity of 180 units was recorded during the presentation of moving and static sound stimuli. Both the activity of single units and the interactions between neighboring neurons in response to each stimulus were analyzed. 2. Sixty-two percent of the units showed significant modulation of their firing rates as a function of the stimulus azimuth. Contralateral stimuli were preferred by the majority (approximately 60%) of these neurons. Thirty-five percent of the units showed mild but statistically significant modulation of their firing rates, which was specifically attributed to the angular movement of the sound source. 3. Eighty-nine percent of the "movement-sensitive" units were also "azimuth sensitive." The sound source's azimuth determined the pattern of the response components (on, sustained, off), whereas the source's movement affected only the magnitude of these components, typically the sustained component. Most neurons for which the sustained response to static sounds was greater for contralateral than ipsilateral stimuli preferred moving sounds that were moving into the contralateral hemifield. 4. Cross-correlation analysis was carried out for 245 neuron pairs. Cross-correlograms were computed for each pair under all stimulus conditions to allow comparison of the neuronal interactions under the various conditions. The shapes of some correlograms (after subtraction of direct stimulus effects) were dependent on specific stimulus conditions, suggesting that the effective connectivity between these neurons depended on the location and/or movement of the sound stimuli. Furthermore, joint peristimulus time (JPST) analysis indicated that modifications of connectivity may be temporally related to the stimulus and may occur over short periods of time. These results could not have been predicted from analysis of the independent single-unit responses to the stimuli. 5. The data suggest that both firing rates and correlated activity between adjacent neurons in the auditory cortex encode sound location and movement.

Acoustic Stimulation↗