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Structure of human auditory cortex. II. Axon distributions and morphological correlates of speech perception.

In Golgi-impregnated specimens of human auditory cortex banding patterns of cortical afferents have been found. Viewed sagitally they are vertical columns with components in layers III, IV, VI and sometimes V. Viewed tangentially they are winding stripes roughly parallel to the gyral axis and of variable width (usually a few hundred micrometers). Although it is not possible to determine it in such sections, they are probably - by analogy with animal experiments - of callosal and/or thalamic origin. Also found were narrow radial bundles, also of indefinite origin. Relative densities of impregnated axons were higher in the columns than between them; also, the tangential orientation component was accentuated within the columns. These findings, together with those of the previous paper, are related to neurolinguistic discoveries. Possible morphological correlates are discussed for neurolinguistic phenomena such as parallel processing of phonemes and words and unilateral, categorical perception of consonants compared with bilateral recognition of vowels and continuous transitions between them.

Aged↗

Resolution of single deviant intervals in periodic stimuli by auditory cortex neurons: comparison of intracochlear electric pulse and acoustic click stimulation.

Responses of neurons in the primary auditory cortex were compared in gerbils receiving intracochlear electric or acoustic stimulation. Stimuli were trains of periodic electric pulses or of acoustic clicks. Interspersed between intervals of equal length were single intervals which were longer, by some Delta t. The Delta t and the repetition rate of these prolonged intervals were varied. The degree of synchronization of spikes to the regular occurrences of prolonged intervals was quantified. While thresholds for synchronized responses to Delta t (at Delta t repetition rates of 4--6 Hz) were about a hundredfold higher for electric (about 5--10 ms) than for acoustic stimulation (about 30 s), Delta t repetition rate response functions were similar for both types of stimulation. The results suggest the feasibility of coding brief acoustic transients by prolonged intervals in electric pulse trains with high pulse repetition rates, which could be another useful strategy for cochlear implants.

Acoustic Stimulation↗

Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus.

We attempt to provide evidence that the projection from the guinea pig auditory cortex (AC) to the inferior colliculus (IC) may contain glutamatergic or GABAergic fibers. Seven days after unilateral AC aspiration, histological studies indicated almost complete AC destruction and preterminal degeneration of fibers and terminal fields in the dorsal cortex (DCIC), external cortex (ECIC), and central nucleus (CNIC) of the IC ipsilateral to the ablated AC. Contralaterally, degeneration appeared in the DCIC. AC ablation depressed the electrically evoked Ca(2+)-dependent release of D-[3H]aspartate (D-[3H]Asp) in the ipsilateral DCIC, ECIC, and CNIC, and D-[3H]Asp uptake in the CNIC. Together with other evidence that the corticocollicular pathway is excitatory, these findings suggest that this projection may contain glutamatergic and/or aspartatergic (Glu/Asp-ergic) fibers. Glutamic acid decarboxylase immunoreactivity was not apparent in presumed pyramidal cells of layer V of the AC retrogradely labeled with biotinylated dextran injected into the ipsilateral IC. Thus, corticocollicular neurons probably do not synthesize GABA and may not be GABAergic. However, AC ablation depressed [14C]GABA release from the ipsilateral DCIC and ECIC, and [14C]GABA uptake in the DCIC. These findings are consistent with the atrophy or down-regulation of some subcortical neurons that mediate GABAergic transmission in the IC.

Aspartic Acid↗

Prenatal and perinatal development of radial cell columns in the human auditory cortex.

The aim of this study was to analyse cytoarchitectonic development of radial cell columns in the human auditory cortex and to correlate these 'ontogenetic' cell columns with the 'adult' pattern of radial cell arrangement. For this cytoarchitectonic analysis, brains were obtained from human fetuses and infants ranging between 9 weeks of gestation and third postnatal month. Plastic and celloidin sections containing prospective auditory areas TC, TB and TA of Economo & Koskinas were stained by Nissl method. In youngest fetuses (8-13 weeks) radially oriented cell columns (1-3 cell wide 'ontogenetic' columns) were found in the whole thickness of the developing cortical plate. During the next developmental stage (13-26 weeks of gestation), radial cell columns were present in the superficial part of the cortical plate, while the deep part of the cortical plate showed a variable cell arrangement due to the formation of the subplate layer (13-15 weeks). The appearance of the pale bands, and development of the prospective granular layer (18-26 weeks). After 28 weeks, parallel to the intensive areal cytoarchitectonic differentiation and ingrowth of callosal afferents, there was a gradual regional rearrangement in the ontogenetic pattern of vertical cell columnation. In the area supratemporalis granulosa (TC), radial columnation was observed as increased granularity and the appearance of short cords composed of drop-like cells. In the area supratemporalis simplex (TB) there was a progressive differentiation of elongated cell columns, intervening fibrillar stripes with appearance of pyramidal cell cords in layers III ('organ pipe' formations).(ABSTRACT TRUNCATED AT 250 WORDS)

Aging↗

Processing of novel sounds and frequency changes in the human auditory cortex: magnetoencephalographic recordings.

Whole-head magnetoencephalographic (MEG) responses to repeating standard tones and to infrequent slightly higher deviant tones and complex novel sounds were recorded together with event-related brain potentials (ERPs). Deviant tones and novel sounds elicited the mismatch negativity (MMN) component of the ERP and its MEG counterpart (MMNm) both when the auditory stimuli were attended to and when they were ignored. MMNm generators were located bilateral to the superior planes of the temporal lobes where preattentive auditory discrimination appears to occur. A subsequent positive P3a component was elicited by deviant tones and with a larger amplitude by novel sounds even when the sounds were to be ignored. Source localization for the MEG counterpart of P3a (P3am) suggested that the auditory cortex in the superior temporal plane is involved in the neural network of involuntary attention switching to changes in the acoustic environment.

Acoustic Stimulation↗

The effects of antioxidants in the senescent auditory cortex.

We investigated whether a 2-month dietary supplementation of antioxidants, in the form of blueberry phytochemicals, could reverse or retard the age-related decline in temporal processing speed observed in the aged rat. To this end, extracellular single unit responses to frequency modulated (FM) sweeps were recorded in the primary auditory cortex (AI) of aged rats that had been placed on either a blueberry-supplemented or control diet 2 months prior to the physiological recordings. Results showed that most cells recorded from the blueberry-fed rats responded most vigorously to fast FM sweeps, similar to that observed in young rats. In contrast, the majority of cells recorded from the control rats showed a preference for slow FM sweep rates. These results suggest that age-related changes in temporal processing speed in A1 may be reversed by dietary supplementation of blueberry phytochemicals.

Action Potentials↗

The non-pyramidal cells in layer III of cat primary auditory cortex (AI).

The form and location of non-pyramidal neurons in layer III of the primary auditory cortex (AI) of adult cats is described in Golgi, Nissl, and other material. The cells were compared to the profiles of retrogradely labeled, commissurally interconnected cells. A principal finding is that certain non-pyramidal and pyramidal cells project interhemispherically to AI; a second conclusion is that the retrogradely labeled commissural cells form small clusters or narrow strips separated by unlabeled patches even after massive injections in the opposite AI. The non-pyramidal cells of origin have not yet been conclusively identified, but they must include one (or more) of the following six types of cells observed in Golgi-impregnated material: tufted or bitufted cells with a radially elongated dendritic arbor; sparsely spinous stellate neurons with thin, smooth dendrites and vertically disposed axonal branches; small stellate cells with varicose dendrites, a restricted dendritic field, and a profusely branched local axon; bipolar neurons with long, thin dendrites; medium-sized multipolar cells with radiating, sparsely branched dendrites; and small stellate neurons with smooth dendrites and a tiny dendritic field. These non-pyramidal cells are found throughout layer III but are more numerous in the upper part, layer IIIa, where they mingle with the small pyramidal neurons. As a rule the axonal branches of non-pyramidal cells are more numerous than those arising from layer III pyramidal neurons, and although they have many axonal collaterals, most project locally and vertically in narrow radial strips. In contrast, pyramidal cell axons have ascending and descending components which invade large, lateral territories in many cortical layers. Layer III non-pyramidal neurons are similar to those in layer IV in certain respects, although their dendritic fields are more spherical and less tufted than those of layer IV cells, and their axons have more local, limited targets. These axons appear to contribute but little to the conspicuous, lateral fiber striae in layer III. The primary intrinsic targets of non-pyramidal cell axons appear to be the apical dendrites of medium-sized and large layer III pyramidal cells, and recurrent branches to the parent cell; their fine, distal branches fortify the vertical plexus in layer III, and certain axons may descend into layer IV. Since layer III in AI receives both commissural and thalamic input, it is possible that these parallel, afferent channels are to some degree segregated, and to some degree convergent, onto particular types of cells.(ABSTRACT TRUNCATED AT 400 WORDS)

Afferent Pathways↗

Spatial focusing of neuronal responses induced by asynchronous two-tone stimuli in the guinea pig auditory cortex.

Spatiotemporal patterns of neuronal responses to asynchronous two-tone stimuli in the anterior field of the auditory cortex of anesthetized guinea pigs were studied using an optical recording method (12 x 12 photodiode array, voltage sensitive dye RH795). Interactions between the onset response to the first tone (masker; 5, 8, 10, 12 and 15 kHz, 200 ms) and to the second tone (probe; 10 kHz, 30 ms) with onset delays relative to the masker onset (0, 5, 10, 15 and 20 ms) were investigated. In general, two-tone interaction was suppressive rather than facilitative. At 0-10 ms probe delays, two-tone responses induced in the probe isofrequency area on the cortex tended to fuse with the masker response. At 15-20 ms probe delays, the probe response was apparently reduced, but was spatially focused and separated from the masker response. This spatial focusing of the probe response may have been due to neuronal inhibition originating after the masker onset response. These results are in agreement with psychoacoustical observations in human subjects, such as auditory segregation, and indicate that the spatial focusing of the cortical response provides a neuronal basis for detecting slightly asynchronous auditory inputs.

Acoustic Stimulation↗

Tonotopic organization of the human auditory cortex.

Neuromagnetic measurements of responses to auditory stimuli consisting of pure tones amplitude-modulated at a low frequency have been used to deduce the location of cortical activity. The evoked field source systematically increased in depth beneath the scalp with increasing frequency of the tone. The tonotopic progression can be described as a logarithmic mapping.

Acoustic Stimulation↗

Harmonic-sensitive neurons in the auditory cortex of the mustache bat.

Human speech and animal sounds contain phonemes with prominent and meaningful harmonics. The biosonar signals of the mustache bat also contain up to four harmonics, and each consists of a long constant-frequency component followed by a short frequency-modulated component. Neurons have been found in a large cluster within auditory cortex of this bat whose responses are facilitated by combinations of two or more harmonically related tones. Moreover, the best frequencies for excitation of these neurons are closely associated with the constant-frequency components of the biosonar signals. The properties of these neurons make them well suited for identifying the signals produced by other echolocating mustache bats. They also show how meaningful components of sound are assembled by neural circuits in the central nervous system and suggest a method by which sounds with important harmonics (or formants) may be detected and recognized by the brain in other species, including humans.

Action Potentials↗

Diversity of receptive field changes in auditory cortex during natural sleep.

Twenty years ago, the study by Livingstone and Hubel [(1981) Nature, 291, 554] was viewed as a first step toward understanding how changes in state of vigilance affect sensory processing. Since then, however, very few attempts have been made to progress in this direction. In the present study, 56 cells were recorded in the auditory cortex of adult, undrugged guinea pigs, and the frequency tuning curves were tested during continuous and stable periods of wakefulness and of slow-wave sleep (SWS). Twelve cells were also tested during paradoxical sleep. Over the whole cell population, the response latency, the frequency selectivity and the size of the suprathreshold receptive field were not significantly modified during SWS compared with waking. However, this lack of global effects resulted from the heterogeneity of response changes displayed by cortical cells. During SWS, the receptive field size varied as a function of the changes in evoked responses: it was unchanged for the cells whose evoked responses were not modified (38% of the cells), reduced for the cells whose responses were decreased (48%) and enlarged for the cells whose responses were increased (14%). This profile of changes differs from the prevalent receptive field shrinkage that was observed in the auditory thalamus during SWS [Edeline et al. (2000), J. Neurophysiol., 84, 934]. It also contrasts with the receptive field enlargement that was described under anaesthesia when the EEG spontaneously shifted from a desynchronized to a synchronized pattern [Wörgötter et al. (1998), Nature, 396, 165]. Reasons for these differences are discussed.

Animals↗

Neural axis representing target range in the auditory cortex of the mustache bat.

In echolocating bats, the primary cue for determining distance to a target is the interval between an emitted orientation sound and its echo. Whereas frequency is represented by place in the bat cochlea, no anatomical location represents of primary range. Target range is coded by the time interval between grouped discharges of primary auditory neurons in response to both the emitted sound and its echo. In the frequency-modulated-signal processing area of the auditory cortex of the mustache bat (Pteronotus parnellii rubiginosus), neurons respond poorly or not at all to synthesized orientation sounds or echoes alone but respond vigorously to echoes following the emitted sound with a specific delay from targets at a specific range. These range-tuned neurons are systemically arranged along the rostrocaudal axis of the frequency-modulated-signal processing area according to the delays to which they best respond, and thus represent target range in terms of cortical organization. The frequency-modulated-signal processing area therefore shows odotopic representation.

Animals↗

Complex tone processing in primary auditory cortex of the awake monkey. I. Neural ensemble correlates of roughness.

Previous physiological studies [e.g., Bieser and Muller-Preuss, Exp. Brain Res. 108, 273-284 (1996); Schulze and Langner, J. Comp. Physiol. A 181, 651-663 (1997); Steinschneider et al., J. Acoust. Soc. Am. 104, 2935-2955 (1998)] have suggested that neural activity in primary auditory cortex (A1) phase-locked to the waveform envelope of complex sounds with low (<300 Hz) periodicities may represent a neural correlate of roughness perception. However, a correspondence between these temporal response patterns and human psychophysical boundaries of roughness has not yet been demonstrated. The present study examined whether the degree of synchronized phase-locked activity of neuronal ensembles in A1 of the awake monkey evoked by complex tones parallels human psychoacoustic data defining the existence region and frequency dependence of roughness. Stimuli consisted of three consecutive harmonics of fundamental frequencies (f(0)s) ranging from 25 to 4000 Hz. The center frequency of the complex tones was fixed at the best frequency (BF) of the cortical sites, which ranged from 0.3 to 10 kHz. Neural ensemble activity in the thalamorecipient zone (lower lamina III) and supragranular cortical laminae (upper lamina III and lamina II) was measured using multiunit activity and current source density techniques and the degree of phase-locking to the f0 was quantified by spectral analysis. In the thalamorecipient zone, the stimulus f0 at which phase-locking was maximal increased with BF and reached an upper limit between 75 and 150 Hz for BFs greater than about 3 kHz. Estimates of limiting phase-locking rates also increased with BF and approximated psychoacoustic values for the disappearance of roughness. These physiological relationships parallel human perceptual data and therefore support the relevance of phase-locked activity of neuronal ensembles in A1 for the physiological representation of roughness.

Animals↗

Optical recording of responses to frequency-modulated sounds in the auditory cortex.

Using an optical recording method with a voltage-sensitive dye, we recorded activities in the primary auditory cortex (AI) of anesthetized guinea pigs in response to frequency-modulated (FM) sounds and sounds with stepwise changes in frequency (SF). Responses to the FM sound showed a spatiotemporal pattern in which a localized active spot traversed the isofrequency bands in the AI, and they differed from the band-like responses to the SF sound. These results indicate that time-varying sounds are represented as spatiotemporal activation of tonotopic organization in the AI by spectral cues with interactions between frequency bands.

Acoustic Stimulation↗

Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus.

Responses of 117 single- or multi-units in the auditory cortex (AC) of bats (Myotis lucifugus) to tone bursts of different stimulus durations (1-400 ms) were studied over a wide range of stimulus intensities to determine how stimulus duration is represented in the AC. 36% of AC neurons responded more strongly to short stimulus durations showing short-pass duration response functions, 31% responded equally to all pulse durations (i.e., all-pass), 18% responded preferentially to stimuli having longer durations (i.e., long-pass), and 15% responded to a narrow range of stimulus durations (i.e., band-pass). Neurons showing long-pass and short-pass duration response functions were narrowly distributed within two horizontal slabs of the cortex, over the rostrocaudal extent of the AC. The effects of stimulus level on duration selectivity were evaluated for 17 AC neurons. For 65% of these units, an increase in stimulus intensity resulted in a progressive decrease in the best duration. In light of the unusual intensity-dependent duration responses of AC neurons, we hypothesized that the response selectivities of AC neurons is different from that in the brainstem. This hypothesis was validated by results of study of the duration response characteristics of single neurons in the inferior colliculus.

Acoustic Stimulation↗

Chandelier cells in the auditory cortex of monkey and man: a Golgi study.

Using the Golgi method we studied chandelier cells in the auditory cortex of monkeys (Macaca irus) subjected to hypoxia before perfusion, and in newborn humans deceased in hypoxic states. In humans these cells have round or ovoid bodies showing usually beaded and sparsely-spined dendrites. These may arise either from both apical and basal poles or from all directions of the soma. With respect to their axons, we found two different types of chandelier cells: cells with extended chandelier complexes which occupied several cortical layers, and cells with local chandelier complexes. The former has rows of vertical terminal endings and the latter has vertical terminals and curved beaded fibers. In adult monkeys, chandelier cells show similar characteristics. The possible relationships between chandelier cells, hypoxia and epilepsy, is discussed.

Adolescent↗