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The inability of squirrel monkeys to localize sound after unilateral ablation of auditory cortex.

The ability of squirrel monkeys to localize brief sounds was tested before and after unilateral ablation of auditory cortex. Results indicated that, after unilateral ablation of auditory cortex, monkeys could no longer localize sound accurately in the hemifield opposite to the side of lesion. These data demonstrate that contralaterally-directed functioning of auditory cortex occurs in primates.

Animals↗

Induction of LTP in the human auditory cortex by sensory stimulation.

High-frequency, repetitive, auditory stimulation was used to determine whether induction of a long-lasting increase of the human auditory evoked potential (AEP) was possible. Recording non-invasively with electroencephalogram scalp electrodes, stable increases in amplitude were observed in the N1 component of the AEP, which is thought to reflect activity within auditory cortex (N1). The increase was maintained over an hour and was shown to be independent of alterations in the state of arousal. This is the first demonstration of the induction of long-lasting plastic changes in AEPs, and suggest that this represents the first direct demonstration of long-term potentiation in the auditory cortex of normal, intact humans.

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Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala.

Single neurons were recorded in freely behaving rats during fear conditioning from areas of auditory cortex that project to the lateral nucleus of the amygdala (LA). The latency and rate of conditioning and extinction were analyzed, and the results were compared to previous recordings from LA itself. Auditory cortex neurons took more trials to learn, and they responded more slowly than LA neurons within trials. Short-latency plasticity in LA, therefore, reflects inputs from the auditory thalamus rather than the auditory cortex. Unlike LA cells, some auditory cortex cells showed late conditioned responses that seemed to anticipate the unconditioned stimulus, while others showed extinction-resistant memory storage. Thus, rapid conditioning of fear responses to potentially dangerous stimuli depends on plasticity in the amygdala, while cortical areas may be particularly involved in higher cognitive (mnemonic and attentional) processing of fear experiences.

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Recovery of function after neonatal ablation of the auditory cortex in rats (Rattus norvegicus).

Functional recovery following neonatal ablation of the auditory cortex was surveyed in 28 rats. Fourteen neonatal-lesioned rats had their temporal cortex lesioned on the date of birth (P1); 7 adult-lesioned rats had their auditory cortex lesioned at P60; and 7 rats served as controls. The training consisted of two phases using task with a Go/No Go procedure. The first task was to detect the presentation of a tone pulse. The second task was to discriminate the pulse rate of a tone pulse. Results showed that the achievements of neonatal-lesioned and control groups were comparable in both tasks. Adult-lesioned rats, however, failed to discriminate temporal patterns, although they could detect tone presentation as efficiently as the other two groups. These findings suggested that discrimination of temporal patterns could be a critical function of the auditory cortex and that brain injury in infancy was more compensated than the comparable damage in adulthood. Neurological plasticity was suggested in the recovery of function in our neonatal-lesioned animals.

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Auditory cortex lesions and discrimination of spatial location by the rat.

Five normal rats and four rats with bilateral lesions of auditory cortex were tested by the conditioned suppression procedure to determine their abilities to discriminate between spatially separated sound sources. The discrimination involved detection of a change in location of a train of clicks from a speaker on the animals' left to a speaker on the right. The separation between speakers was varied from 180 degrees to 90 degrees, 45 degrees, 22 degrees, 12 degrees, 6 degrees, and psychophysical functions were obtained using a method of descending limits. Both normal and brain-damaged animals were capable of discriminating left from right clicks and psychophysical curves were similar for the two groups. Histological analysis indicated that the lesions in each of the four brain-damaged rats destroyed primary auditory cortex as well as surrounding belt areas. Therefore, for the rat, auditory cortex was not found to be essential for discrimination of the spatial locations of auditory stimuli. The results are discussed in light of impairments in sound localization following lesions of auditory cortex in other mammalian species.

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Corticocortical connections of cat primary auditory cortex (AI): laminar organization and identification of supragranular neurons projecting to area AII.

The laminar distribution and structure of the supragranular cells projecting from primary auditory cortex (AI) to the second auditory cortex (AII) in the cat were studied with horseradish peroxidase. Injections in AII retrogradely labeled somata in ipsilateral cortical layers I-VI of AI. A bimodal laminar disposition was found, with approximately 40% of the labeled cells in layer III, 25% in layer V, and 10-15% each in layers II, IV, and VI; only a few cells were found in layer I. The labeled cells were scattered in small aggregates between which unlabeled neurons were interspersed. There was some, though not a strict, topographical distribution of the labeled cells according to the locus of the injection in AII. Injections in the caudal part of AII labeled cells in more rostral AI, while rostral AII injections labeled cells in more caudal AI. Ventral AII injections labeled more ventrally located AI cells, while more dorsal AII injections labeled more dorsally situated AI cells. AII injections also labeled cells in other auditory cortex subdivisions, including the posterior ectosylvian, ventroposterior, temporal, and dorsal auditory zone/suprasylvian fringe cortical areas, and in some non-auditory cortical areas. In layers II and III, both pyramidal and non-pyramidal cells were labeled. More pyramidal cells were labeled in layer III than layer II (80% vs. 62%), and the proportion of non-pyramidal cells in layer II was more than twice that in layer IV (27% vs. 12%). The types of labeled cells were distinguished from one another on the basis of size, somatic and dendritic shape, and laminar distribution. The profiles of labeled cells in these experiments were compared to, and correlated with, those in Golgi-impregnated material. In layer II, the classes of corticocortical projecting cells consisted of small and medium-sized pyramidal, bipolar, and multipolar cells. Those in layer III included small, medium-sized, and large pyramidal neurons, and bipolar and multipolar cells. The average somatic area of the labeled cells did not differ significantly from that of the unlabeled cells, and both were about equal in somatic size to neurons accumulating tritiated gamma-aminobutyric acid in layers II and III. These findings suggest that there is convergent, ipsilateral input onto AII from every layer in AI, and from other cortical auditory and non-auditory areas. A morphologically heterogeneous population of cells in AI contributes to these projections. Diversity in the cytological origins of corticocortical projections implies functional differences between layers II and III since the latter also projects commissural, while layer II in the cat, does not.

Animals↗

Fine functional organization of auditory cortex revealed by Fourier optical imaging.

We provide an overall view of the functional tonotopic organization of the auditory cortex in the rat. We apply a recently developed technique for acquiring intrinsic signal optical maps, Fourier imaging, in the rat auditory cortex. These highly detailed maps, derived in a several-minute-long recording procedure, delineate multiple auditory cortical areas and demonstrate their shapes, sizes, and tonotopic order. Beyond the primary auditory cortex, there are at least three distinct areas with fine-scale tonotopic organization, as well as at least one additional high-frequency field. The arrangement of all of these cortical areas is consistent across subjects. The accuracy of these optical maps was confirmed by microelectrode mapping in the same subjects. This imaging method allows fast mapping of the auditory cortex at high spatial resolution comparable to that provided by conventional microelectrode technique. Although spiking activity is largely responsible for the evoked intrinsic signals, certain features of the optical signal cannot be explained by spiking activity only, and should probably be attributed to other mechanisms inducing metabolic activity, such as subthreshold membrane phenomena.

Animals↗

Nonauditory events of a behavioral procedure activate auditory cortex of highly trained monkeys.

A central tenet in brain research is that early sensory cortex is modality specific, and, only in exceptional cases, such as deaf and blind subjects or professional musicians, is influenced by other modalities. Here we describe extensive cross-modal activation in the auditory cortex of two monkeys while they performed a demanding auditory categorization task: after a cue light was turned on, monkeys could initiate a tone sequence by touching a bar and then earn a reward by releasing the bar on occurrence of a falling frequency contour in the sequence. In their primary auditory cortex and posterior belt areas, we found many acoustically responsive neurons whose firing was synchronized to the cue light or to the touch or release of the bar. Of 315 multiunits, 45 exhibited cue light-related firing, 194 exhibited firing that was related to bar touch, and 268 exhibited firing that was related to bar release. Among 60 single units, we found one neuron with cue light-related firing, 21 with bar touch-related firing, and 36 with release-related firing. This firing disappeared at individual sites when the monkeys performed a visual detection task. Our findings corroborate and extend recent findings on cross-modal activation in the auditory cortex and suggests that the auditory cortex can be activated by visual and somatosensory stimulation and by movements. We speculate that the multimodal corepresentation in the auditory cortex has arisen from the intensive practice of the subjects with the behavioral procedure and that it facilitates the performance of audiomotor tasks in proficient subjects.

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Influence of urethane anesthesia on neural processing in the auditory cortex analogue of a songbird.

Functional maps of auditory response areas were derived from multi-unit recordings in the caudal telencephalon of the starling (Sturnus vulgaris L.). A regular grid of recording sites with distances of 200 microns horizontally and 100 microns vertically was placed over the auditory cortex analogue. Within one plane, mapping of auditory responses was first performed in the awake bird and then repeated under urethane anesthesia. The data from both experimental approaches differ considerably. Urethane reduces the spontaneous discharge rate significantly. Under anesthesia, inhibition decreases in all auditory subunits. Excitation is less affected. Eight auditory subcenters were divided into three groups according to the changes in their excitatory responses. In the first group 'on' and sustained excitation changed only weakly. These areas are thought to receive direct inputs from the diencephalon. In the second group, 'on' and sustained excitation are substantially reduced. These subcenters seem to receive projections from other forebrain areas. In subunits of the third group, an increase in sustained excitation is correlated to a decrease in inhibition. Within some specific centers, distinct natural calls, for example the bird's own song, elicit stronger responses under anesthesia than other stimuli.

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Primary and secondary auditory cortex stimulation for intractable tinnitus.

INTRODUCTION: Recent research suggests tinnitus is a phantom phenomenon based on hyperactivity of the auditory system, which can be visualized by functional neuroimaging, and transiently modulated by transcranial magnetic stimulation (TMS). We present the results of the first implanted electrodes on the primary and secondary auditory cortex after a successful TMS suppression. METHODS AND MATERIALS: Twelve patients underwent an auditory cortex implantation, 10 for unilateral and 2 for bilateral tinnitus, based on >50% suppression applying TMS. Results were analyzed for pure tone tinnitus and white noise tinnitus. RESULTS: TMS results in 77% pure tone tinnitus and 67% white noise reduction. Electrical stimulation via an implanted electrode results in a mean of 97% pure tone tinnitus and 24% white noise suppression. Mean Visual Analogue Scale score decreases from 9.5 to 1.5 for pure tone and from 8.8 to 6.8 for white noise postoperatively. DISCUSSION: Pure tone tinnitus might be the conscious percept of focal neuronal hyperactivity of the auditory cortex. Once visualized, this hyperactivity can be modulated by neurostimulation. CONCLUSION: The preliminary results of the first implantations suggest that patients with unilateral pure tone tinnitus are good surgical candidates for electrode implantation and permanent electrical stimulation of the auditory cortex, provided that the tinnitus is of recent origin and can be suppressed by TMS.

Adult↗

[Quantitative and qualitative characteristics of synapses in different layers of the auditory cortex].

The electron-microscopic examination of synapses in different layers of the cat auditory cortex was performed. 53% of them were located on dendritic spines, 37% on dendrites and 10% on neuronal soma. All synapses were separated into type I and type II according to Gray. The type I synapses amounted to 91% (69.5% were of type Ia and 21.5% of type Ib), the type II synapses constituted 9%. The type I synapses were located mainly on dendrites and dendritic spines, the type II--on neuronal soma, axon hillocks and large dendrites. 60 h after complete neuronal isolation of a portion of the auditory cortex 22.8% of synapses revealed signs of degeneration. No type II degenerating synapses were found. This indicates that they are formed by axons of intracortical neurons. Quantitative and qualitative composition of synapses in different layers of the auditory cortex is shown to be different.

Animals↗

High metabolic activity demonstrated by positron emission tomography in human auditory cortex in case of deafness of early onset.

Glucose metabolism has been studied in the auditory cortex of human subjects with deafness of early onset, and compared to normal subjects with ears plugged. The metabolism in the auditory cortex and in the association auditory cortex was higher in deaf subjects than in normal subjects. This result is compared to similar observations that we made previously in the visual cortex of human subjects with blindness of early onset.

Adolescent↗

Frequency and space representation in the primary auditory cortex of the frequency modulating bat Eptesicus fuscus.

1. Frequency and space representation in the auditory cortex of the big brown bat, Eptesicus fuscus, were studied by recording responses of 223 neurons to acoustic stimuli presented in the bat's frontal auditory space. 2. The majority of the auditory cortical neurons were recorded at a depth of less than 500 microns with a response latency between 8 and 20 ms. They generally discharged phasically and had nonmonotonic intensity-rate functions. The minimum threshold, (MT) of these neurons was between 8 and 82 dB sound pressure level (SPL). Half of the cortical neurons showed spontaneous activity. All 55 threshold curves are V-shaped and can be described as broad, intermediate, or narrow. 3. Auditory cortical neurons are tonotopically organized along the anteroposterior axis of the auditory cortex. High-frequency-sensitive neurons are located anteriorly and low-frequency-sensitive neurons posteriorly. An overwhelming majority of neurons were sensitive to a frequency range between 30 and 75 kHz. 4. When a sound was delivered from the response center of a neuron on the bat's frontal auditory space, the neuron had its lowest MT. When the stimulus amplitude was increased above the MT, the neuron responded to sound delivered within a defined spatial area. The response center was not always at the geometric center of the spatial response area. The latter also expanded with stimulus amplitude. High-frequency-sensitive neurons tended to have smaller spatial response areas than low-frequency-sensitive neurons. 5. Response centers of all 223 neurons were located between 0 degrees and 50 degrees in azimuth, 2 degrees up and 25 degrees down in elevation of the contralateral frontal auditory space. Response centers of auditory cortical neurons tended to move toward the midline and slightly downward with increasing best frequency. 6. Auditory space representation appears to be systematically arranged according to the tonotopic axis of the auditory cortex. Thus, the lateral space is represented posteriorly and the middle space anteriorly. Space representation, however, is less systematic in the vertical direction. 7. Auditory cortical neurons are columnarly organized. Thus, the BFs, MTs, threshold curves, azimuthal location of response centers, and auditory spatial response areas of neurons sequentially isolated from an orthogonal electrode penetration are similar.

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Some functions of primary auditory cortex in learning and memory formation.

In the primary auditory field AI of gerbil auditory cortex, aversive tone conditioning paradigms reshaped frequency receptive fields of single units and also changed the spatial representation of tones in fluoro-2-deoxyglucose (FDG) experiments. As another aspect of learning-induced plasticity in gerbil AI, antibodies against the immediate early gene product c-Fos identified an unusual spatial pattern of neurons in terms of a "macrocolumn." The pattern resulted from repeated short exposure of the animals to a tone in a new environment. The search for transmitters that may mediate this gene activation is carried out by microdialysis through chronically implanted probes in auditory cortex. So far, dopamine transmission was found to reflect specific aspects of auditory learning in cortex. The results suggest that spectral features of sounds as well as aspects of learned behavioral meaning of the sounds may be represented in AI.

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An immunocytochemical mapping of somatostatin in the cat auditory cortex.

Using an indirect immunoperoxidase technique, the localization of somatostatin-28 (1-12)-like immunoreactive fibers and cell bodies in the auditory cortex of the cat (anterior, primary, secondary, temporal, ventral, ventroposterior, posterior and dorsoposterior auditory fields) was studied. In general, the distribution of SOM-ir structures is widespread in the auditory cortex of the feline. A high density of immunoreactive fibers as well as a low density of cell bodies containing somatostatin were observed in all the layers of the eight above-mentioned auditory fields. These data indicate that somatostatin-28 (1-12) could act as a neurotransmitter and/or a neuromodulator in the auditory cortex of the cat. The origin of the SOM-ir fibers in the auditory cortex of the cat, as well as the issue of whether the cell bodies containing somatostatin-28 (1-12) are local or projecting neurons is discussed.

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Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections.

The auditory cortex of the Mongolian gerbil comprises several physiologically identified fields, including the primary (AI), anterior (AAF), dorsal (D), ventral (V), dorsoposterior (DP) and ventroposterior (VP) fields, as established previously with electrophysiological [Thomas et al. (1993) Eur. J. Neurosci., 5, 882] and functional metabolic techniques [Scheich et al. (1993) Eur. J. Neurosci., 5, 898]. Here we describe the cyto-, myelo- and chemoarchitecture and the corticocortical connections of the auditory cortex in this species. A central area of temporal cortex corresponding to AI and the rostrally adjacent AAF is distinguished from surrounding cortical areas by its koniocortical cytoarchitecture, by a higher density of myelinated fibres, predominantly in granular and infragranular layers, and by characteristic patterns of immunoreactivity for the calcium-binding protein parvalbumin (most intense staining in layers III/IV and VIa) and for the cytoskeletal neurofilament protein (antibody SMI-32; most intense staining in layers III, V and VI). Concerning the cortical connections, injections of the predominantly anterograde tracer biocytin into the four tonotopically organized fields AI, AAF, DP and VP yielded the following labelling patterns. (i) Labelled axons and terminals were seen within each injected field itself. (ii) Following injections into AI, labelled axons and terminals were also seen in the ipsilateral AAF, DP, VP, D and V, and in a hitherto undescribed possible auditory field, termed the ventromedial field (VM). Similarly, following injections into AAF, DP and VP, labelling was also seen in each of the noninjected fields, except in VM. (iii) Each field projects to its homotopic counterpart in the contralateral hemisphere. In addition, field AI projects to contralateral AAF, DP and VP, field DP to contralateral AI and VP, and field VP to contralateral AI and DP. (iv) Some retrogradely filled pyramidal neurons within the areas of terminal labelling indicate reciprocal connections between most fields, both ipsilateral and contralateral. (v) The labelled fibres within the injected and the target fields, both ipsilateral and contralateral, were arranged in continuous dorsoventral bands parallel to isofrequency contours. The more caudal the injection site in AI the more rostral was the label in AAF. This suggests divergent but frequency-specific connections within and, at least for AI and AAF, also across fields, both ipsilateral and contralateral. (vi) Projections to associative cortices (perirhinal, entorhinal, cingulate) and to other sensory cortices (olfactory, somatosensory, visual) from AAF, DP and VP appeared stronger than those from AI. These data support the differentiation of auditory cortical fields in the gerbil into at least 'core' (AI and AAF) and 'noncore' fields. They further reveal a complex pattern of interconnections within and between auditory cortical fields and other cortical areas, such that each field of auditory cortex has its unique set of connections.

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Developmental hemispheric asymmetry of interregional metabolic correlation of the auditory cortex in deaf subjects.

The functional connectivity of the auditory cortex might be altered in deaf subjects due to the loss of auditory input. We studied the developmental changes of functional connectivity of the primary auditory cortex (A1) in deaf children, deaf adults, and normal hearing adults by examining interregional metabolic correlation with (18)F-FDG PET. The mean activity of FDG uptake in the cytoarchitectonically defined A1 region served as a covariate in the interregional and interhemispheric correlation analysis. A1 metabolic rate was correlated with that of the ipsilateral superior temporal lobe in both normal and deaf subjects. This correlated area was larger in deaf children than in deaf or normal hearing adults. Concerning the functional connectivity of A1, a hemispheric asymmetry was found in that the extent of interregional correlation was clearly larger in the right than in the left hemisphere. This asymmetry was particularly pronounced in the younger deaf children. Both extent and asymmetry of the functional connectivity of A1 subsided with age. Contrary to this, a correlation between the left and the right primary auditory cortices was absent in younger deaf children but became apparent as they grew older.

Adolescent↗

Tone-evoked oscillations in the rat auditory cortex result from interactions between the thalamus and reticular nucleus.

This study investigates the origins of tone-evoked oscillations (5-13 Hz) in the thalamo-cortical auditory system of anaesthetized rats. In three separate experiments, the auditory sector of the reticular nucleus (RE), the auditory cortex and the auditory thalamus were inactivated by local applications of muscimol (1 mg/mL). To assess the efficacy of this procedure, recordings were performed in the inactivated structure in each experiment; and to determine the extent of the drug diffusion autoradiographic experiments were carried out. The evolution of the strength of the oscillations was followed using power spectra during the whole recording session. In the first experiment, muscimol injection in the auditory RE totally suppressed the tone-evoked oscillations in the auditory thalamus and cortex. In the second experiment, inactivation of the auditory cortex did not interfere with the presence of tone-evoked oscillations in the auditory RE. In the third experiment, inactivation of the auditory thalamus impaired the oscillations produced by cortical stimulation in the auditory RE. From these results, it appears that both the auditory thalamus and the auditory sector of the RE, but not the auditory cortex, are involved in the generation of stimulus-evoked oscillations in the thalamo-cortical auditory system.

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