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PubMed1985

Structure of layer II in cat primary auditory cortex (AI).

The cytoarchitecture, myeloarchitecture, neuronal architecture, and intrinsic and laminar organization of layer II were studied in the primary auditory cortex (AI) of adult cats. The chief goal was to describe the different types of cells and axons to provide a framework for experimental studies of corticocortical connections or of neurons accumulating putative neurotransmitters. A further goal was to differentiate layer II from layer III. Layer II extends from 150-200 micron to about 400 micron beneath the pia and has two subparts. The superficial stratum, layer IIa, has many small, chiefly non-pyramidal neurons, primarily with round or oval perikarya, and a sparse, fine, and irregularly arranged axonal plexus. Layer IIb somata are larger and more densely packed and there is a more developed vertical and lateral axonal plexus. The border with layer III was marked by numerous large pyramidal cells with a thicker apical dendrite with more developed basal dendritic arbors than those of layer II pyramidal cells. Eight varieties of neurons were recognized in Golgi-impregnated material. These included small and medium-sized pyramidal cells, whose apical dendrites often ramified in layer I; bipolar and bitufted cells with polarized, sparse dendritic arbors; small smooth or sparsely spinous multipolar cells with radiating dendrites and small dendritic fields; spinous multipolar cells, whose large dendritic fields had more extensive apical than basal arbors; large sparsely spinous multipolar cells with smooth, robust apical dendrites; tufted multipolar cells with highly developed apical dendrites and some dendritic appendages; and extraverted multipolar cells with a broad, candelabra-shaped dendritic configuration, and with most dendrites oriented at right angles to the pia. The axons of the different cell types had the following general dispositions: those arising from the pyramidal cells could often be traced into the white matter but had many local branches as well; those of the other neurons had more or less extensive local axonal collateral systems and fewer branches which appeared to be corticofugal. However, the complete trajectory of the axons was not always impregnated in the adult material.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗
PubMed1990

Functional topography of cat primary auditory cortex: distribution of integrated excitation.

1. Neuronal responses to tones and transient stimuli were mapped with microelectrodes in the primary auditory cortex (AI) of barbiturate anesthetized cats. Most of the dorsoventral extent of AI was mapped with multiple-unit recordings in the high-frequency domain (between 5.8 and 26.3 kHz) of all six studied cases. The spatial distributions of 1) sharpness of tuning measured with pure tones and 2) response magnitudes to a broadband transient were determined in each of three intensively studied cases. 2. The sharpness of tuning of integrated cluster responses was defined 10 dB above threshold (Q10 dB, integrated excitatory bandwidth). The spatial reconstructions revealed a frequency-independent maximum located near the center of the dorsoventral extent of AI. The sharpness of tuning gradually decreased toward the dorsal and ventral border of AI in all three cases. 3. The sharpness of tuning 40 dB above response threshold was also analyzed (Q40 dB). The Q40 dB values were less than one-half of the corresponding Q10 dB value. The spatial distribution showed a maximum in the center of AI, similar to the Q10 dB distribution. In two out of three cases, restricted additional maxima were recorded dorsal to the main maximum. Overall, Q10 dB and Q40 dB were only moderately correlated, indicating that the integrated excitatory bandwidth at higher stimulus levels can be influenced by additional mechanisms that are not active at lower levels. 4. The magnitude of excitatory responses to a broadband transient (frequency-step response) was determined. The normalized response magnitude varied between less than 1% and up to 100% relative to a characteristic frequency (CF) tone response. The step-response magnitude showed a systematic spatial distribution. An area dorsal to the Q10 dB maximum consistently showed the largest response magnitude surrounded by areas of lower responsivity. A second spatially more restricted maximum was recorded in the ventral-third of each map. Areas with high-transient responsiveness coincided with areas of broad integrated excitatory bandwidth at comparable stimulus levels. 5. The distribution of excitation produced by narrowband and broadband signals suggest that there exists a clear functional organization in the isofrequency domain of AI that is orthogonal to the main cochleotopic organization of the AI. Systematic spatial variations of the integrated excitatory bandwidth reflect underlying cortical processing capacities that may contribute to a parallel analysis of spectral complexity, e.g., spectral shape and contrast, at any given frequency.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation↗
PubMed1994

Single thalamocortical axons diverge to multiple patches in neonatal auditory cortex.

Thalamic afferents originating in the ventral division of the medial geniculate body (vMGB) terminate in patches within lamina III/IV of the primary auditory cortex in adult rabbits. Focal iontophoretic injections of the anterograde tracer, biocytin, were made into the vMGB of neonatal rabbits to examine the morphological organization of auditory thalamocortical (TC) afferents prior to hearing onset. TC afferents terminated in distinct patches as early as postnatal day 1 (PD-0 = day of birth), 6 days before the behavioral onset of hearing. In contrast to TC afferents in adults, the terminal arbors of neonatal vMGB axons occupied the entire depth of the cortical plate and lamina I. Serial section reconstructions revealed that single vMGB axons in neonates branched to form multiple patches within the cortical plate. Collaterals also extended to lamina I where they coursed tangentially for several millimeters. An unusual feature of the neonatal TC patches was the contribution of descending collaterals from axons coursing in lamina I. The presence of distinct patches prior to hearing onset indicates that the segregation of auditory TC axons occurs in the absence of acoustically driven activity. The extensive postnatal remodeling of TC axons, however, may indicate activity-dependent refinement of arbor size.

Animals↗
PubMed2003

Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss.

Increase in spontaneous neural activity after noise-induced hearing loss has frequently been associated with the phenomenon of tinnitus. Eighteen juvenile and adult cats were exposed for 2 h to a 6 kHz tone with an intensity of 115 dB SPL at the cat's head. Seven non-exposed littermates and seven other normal hearing cats were used as age-matched controls. The trauma cats showed localized hearing losses, as assessed by ABR, ranging from less than 20 to 60 dB. The frequency representation in primary auditory cortex was mapped using an eight-electrode array. Single-unit spontaneous activity was recorded for 15 min. Peak cross-correlation coefficients (R) for unit cluster activity recorded on separate electrodes were calculated. We found elevated spontaneous firing rates in regions with reorganization of the tonotopic map compared to the neurons in the non-reorganized cortical regions in the same animals. A second finding was that in these regions the peak cross-correlation coefficients were also increased relative to the non-reorganized parts. A third finding was that exposed animals showed higher spontaneous activity compared to controls regardless of the presence of cortical reorganization. This may be a correlate of tinnitus in the presence of only minor hearing losses.

Acoustic Stimulation↗
PubMed2006

Projections from auditory cortex to cochlear nucleus: A comparative analysis of rat and mouse.

Mammalian hearing is a complex special sense that involves detection, localization, and identification of the auditory stimulus. The cerebral cortex may subserve higher auditory processes by providing direct modulatory cortical projections to the auditory brainstem. To support the hypothesis that corticofugal projections are a conserved feature in the mammalian brain, this article reviews features of the rat corticofugal pathway and presents new data supporting the presence of similar projections in the mouse. The mouse auditory cortex was localized with electrophysiological recording and neuronal tracers were injected into AI. The cochlear nucleus was dissected and examined for terminal fibers by light and electron microscopy. Bouton endings were found bilaterally forming synapses with dendrites of granule cells of the cochlear nucleus. This report provides evidence for direct auditory cortex projections to the cochlear nucleus in the mouse. The distribution of projections to the granule cell domain and the synapses onto granule cell dendrites are consistent with what has been reported for rats and guinea pigs. These findings suggest a general plan for corticofugal modulation of ascending auditory information in mammals. Corticobulbar inputs to the auditory brainstem likely provided a survival advantage by improving sound detection and identification, thus allowing the development of complex social behaviors and the navigation of varied environments.

Animals↗
PubMedDate not supplied

[Inhibitory processes in neuronal reactions of the auditory cortex in the cat undergoing dichotic stimulation].

In experiments on anaesthetized cats, studies have been made of intracellular and extracellular responses of single units in the auditory cortex during dichotic stimulation simulating sound source motion. Responses of some cortical units exhibit strong dependence on the signal parameters related to spatial and directional characteristics of simulated sound source motion. Profound inhibition was invariably revealed at the beginning of sonic stimulation as well as during certain moments of its movement. The role of inhibition in formation of cortical reactions to sound source motion is discussed.

Acoustic Stimulation↗
PubMed2005

Modulation of gamma-aminobutyric acid type A receptor-mediated spontaneous inhibitory postsynaptic currents in auditory cortex by midazolam and isoflurane.

BACKGROUND: Anesthetic agents that target gamma-aminobutyric acid type A (GABA(A)) receptors modulate cortical auditory evoked responses in vivo, but the cellular targets involved are unidentified. Also, for agents with multiple protein targets, the relative contribution of modulation of GABA(A) receptors to effects on cortical physiology is unclear. The authors compared effects of the GABA(A) receptor-specific drug midazolam with the volatile anesthetic isoflurane on spontaneous inhibitory postsynaptic currents (sIPSCs) in pyramidal cells of auditory cortex. METHODS: Whole cell recordings were obtained in murine brain slices at 34 degrees C. GABA(A) sIPSCs were isolated by blocking ionotropic glutamate receptors. Effects of midazolam and isoflurane on time course, amplitude, and frequency of sIPSCs were measured. RESULTS: The authors detected no effect of midazolam at 0.01 microM on sIPSCs, whereas midazolam at 0.1 and 1 microM prolonged the decay of sIPSCs by approximately 25 and 70%, respectively. Isoflurane at 0.1, 0.25, and 0.5 mm prolonged sIPSCs by approximately 45, 150, and 240%, respectively. No drug-specific effects were observed on rise time or frequency of sIPSCs. Isoflurane at 0.5 mm caused a significant decrease in sIPSC amplitude. CONCLUSIONS: The dose dependence of isoflurane effects on GABA(A) sIPSCs in pyramidal cells is consistent with effects on auditory evoked response in vivo. By contrast, comparable effects of midazolam on GABA(A) sIPSCs arise at concentrations exceeding those currently thought to be achieved in vivo, suggesting that the cellular targets of midazolam reside elsewhere in the thalamocortical circuit or that the concentration of midazolam reached in the brain is higher than currently believed.

Anesthetics, Inhalation↗
PubMed2004

Stimulus dependence of spectro-temporal receptive fields in cat primary auditory cortex.

The frequency-tuning curve is a static representation of the neuron's sensitivity to stimulus frequency. The temporal aspects of the frequency sensitivity can be captured in the spectro-temporal receptive field (STRF), often presented as the average spectrogram of the stimulus preceding a spike but also as the average frequency-dependent post-stimulus time histogram (PSTH). The temporal envelope of the stimulus produces considerable smoothing, and as a consequence the PSTH representation is finer-grained than the spectrogram representation. Here we compare STRFs for 1/s and 20/s single-frequency stimuli with 120/s steady-state multi-frequency stimuli for 87 recording sites in primary auditory cortex of cats. For the 672 estimated STRFs, which for multi-frequency stimuli were mostly obtained at 55 dB SPL, we found lateral inhibition in 17% of the cases, in 32% post-activation suppression, and in 51% only excitation. In 35% of the recordings the excitatory frequency-tuning curves were very similar for single and multi-frequency stimuli, in the remaining 65% the common finding was the emergence of an intensity independent bandwidth for the multi-frequency stimuli. Comparison of the 20/s and 120/s stimuli showed that the resulting increase in inhibition was strongest in the center of the STRF.

Acoustic Stimulation↗
PubMed1998

Pitch vs. spectral encoding of harmonic complex tones in primary auditory cortex of the awake monkey.

Neuromagnetic studies in humans and single-unit studies in monkeys have provided conflicting views regarding the role of primary auditory cortex (A1) in pitch encoding. While the former support a topographic organization based on the pitch of complex tones, single-unit studies support the classical tonotopic organization of A1 defined by the spectral composition of the stimulus. It is unclear whether the incongruity of these findings is due to limitations of noninvasive recordings or whether the discrepancy genuinely reflects pitch representation based on population encoding. To bridge these experimental approaches, we examined neuronal ensemble responses in A1 of the awake monkey using auditory evoked potential (AEP), multiple-unit activity (MUA) and current source density (CSD) techniques. Macaque monkeys can perceive the missing fundamental of harmonic complex tones and therefore serve as suitable animal models for studying neural encoding of pitch. Pure tones and harmonic complex tones missing the fundamental frequency (f0) were presented at 60 dB SPL to the ear contralateral to the hemisphere from which recordings were obtained. Laminar response profiles in A1 reflected the spectral content rather than the pitch (missing f0) of the compound stimuli. These findings are consistent with single-unit data and indicate that the cochleotopic organization is preserved at the level of A1. Thus, it appears that pitch encoding of multi-component sounds is more complex than suggested by noninvasive studies, which are based on the assumption of a single dipole generator within the superior temporal gyrus. These results support a pattern recognition mechanism of pitch encoding based on a topographic representation of stimulus spectral composition at the level of A1.

Acoustic Stimulation↗
PubMed1994

Speech-evoked activity in primary auditory cortex: effects of voice onset time.

Neural encoding of temporal speech features is a key component of acoustic and phonetic analyses. We examined the temporal encoding of the syllables /da/ and /ta/, which differ along the temporally based, phonetic parameter of voice onset time (VOT), in primary auditory cortex (A1) of awake monkeys using concurrent multilaminar recordings of auditory evoked potentials (AEP), the derived current source density, and multiunit activity. A general sequence of A1 activation consisting of a lamina-specific profile of parallel and sequential excitatory and inhibitory processes is described. VOT is encoded in the temporal response patterns of phase-locked activity to the periodic speech segments and by "on" responses to stimulus and voicing onset. A transformation occurs between responses in the thalamocortical (TC) fiber input and A1 cells. TC fibers are more likely to encode VOT with "on" responses to stimulus onset followed by phase-locked responses during the voiced segment, whereas A1 responses are more likely to exhibit transient responses both to stimulus and voicing onset. Relevance to subcortical speech processing, the human AEP and speech psychoacoustics are discussed. A mechanism for categorical differentiation of voiced and unvoiced consonants is proposed.

Animals↗
PubMed2000

Neuronal responses in cat primary auditory cortex to natural and altered species-specific calls.

We investigated how natural and morphed cat vocalizations are represented in primary auditory cortex (AI). About 40% of the neurons showed time-locked responses to major peaks in the vocalization envelope, 60% only responded at the onset. Simultaneously recorded multi-unit (MU) activity of these peak-tracking neurons on separate electrodes was significantly more synchronous during stimulation than under silence. Thus, the representation of the vocalizations is likely synchronously distributed across the cortex. The sum of the responses to the low and high frequency part of the meow, with the boundary at 2.5 kHz, was larger than the neuronal response to the natural meow itself, suggesting that strong lateral inhibition is shaping the response to the natural meow. In this sense, the neurons are combination-sensitive. The frequency-tuning properties and the response to amplitude-modulated tones of the MU recordings can explain the responses to natural, and temporally and spectrally altered vocalizations. Analysis of the mutual information in the firing rate suggests that the activity of at least 95 recording sites in AI would be needed to reliably distinguish between the nine different vocalizations. This suggests that a distributed representation based on temporal stimulus aspects may be more efficient than one based on firing rate.

Acoustic Stimulation↗
PubMed2006

Response to broadband repetitive stimuli in auditory cortex of the unanesthetized rat.

This study examines the ability of multi-unit clusters (MUCs) in layer IV/V of primary auditory cortex of the awake rat to respond to a series of broadband click trains. The data from 113 multi-unit clusters were analyzed for synchronous and nonsynchronized responses using several methods. Synchronous responses were measured using window analysis, circular statistics and spectral analysis. Nonsynchronous responses were measured during different time intervals during the click train (first 50 ms, 50-450 ms, and the entire click train). The results demonstrate that multi-unit clusters are capable of synchronizing to clicks at rates up to 166 Hz. The mean synchronization boundary (limiting rate) for the group was found to be 72 Hz. Mean peak response rate, mean response duration, and mean time-to-peak response decreased as the stimulus presentation rate (SPR) increased, resulting in a temporal sharpening of the population response. For fast SPRs (>50 Hz), 50% of MUCs exhibited nonsynchronous responses in which the firing rate increased with SPR, although this activity was most prevalent during the first 50 ms of the response. Sustained increases in firing rate with SPR were seen in 8% of the MUCs, while another 38% of MUCs exhibited sustained decreases during the click train.

Acoustic Stimulation↗
PubMed2001

Reorganization in awake rat auditory cortex by local microstimulation and its effect on frequency-discrimination behavior.

In common with other sensory cortices, the mammalian primary auditory cortex (AI) demonstrates the capacity for large-scale reorganization following many experimental situations. For example, training animals in frequency-discrimination tasks has been shown to result in an increase in cortical frequency representation. Such central changes-most commonly, an increase in central representation of specific stimulus parameters-have been hypothesized to underlie the improvements in perceptual acuity (perceptual learning) seen in many learning situations. The actual behavioral relevance of central reorganizations, however, remains speculative. Here, we directly examine this issue. We first show that stimulating the AI cortex of the awake rat with a weak electric current (intracortical microstimulation or ICMS) has the effect of inducing central reorganizations similar to those accompanying the traditional plasticity experiments (a result previously noted only in anesthetized preparations). Depending on the site of AI stimulation, ICMS enlarged the cortical representation of certain frequencies. Next we examined the direct perceptual consequences of ICMS-induced AI reorganization for the rat's ability to discriminate frequencies. Over the course of the experiment, we also detailed, and made comparisons between, the frequency-response characteristics of rat AI cortex in the awake and ketamine-anesthetized animal. AI cells that responded to pure tones were divided into two categories--strongly and weakly responsive--based on the strength of their evoked discharge. Individual cells maintained their respective response strengths in both awake and anesthetized conditions. Strongly responsive cells showed at least four different temporal responses and tended to be narrowly tuned. Their responses were stable over the long term. In general frequency-response characteristics were qualitatively similar in the anesthetized and awake animal; bandwidths tended to be broader in awake animals. Although both strong and weak cell populations respond to tones, only the strongly responsive cells fit into a tonotopically organized scheme. By contrast, weakly responsive cells did not exhibit a frequency mapping and may represent a more diffuse input to AI than that underlying strongly responsive cells. In general, the overall frequency organization of AI was found to be equally well expressed in both the awake and anesthetized rat. ICMS reorganization of AI did not alter frequency-discrimination behavior in the rat--either signal detectability or response bias--suggesting that an increase in central representation, by itself, is insufficient to account for perceptual learning. It is likely that cortical reorganizations that accompany perceptual learning are strongly keyed to specific behavioral contexts.

Acoustic Stimulation↗
PubMed2003

Topography and synaptic shaping of direction selectivity in primary auditory cortex.

The direction of frequency-modulated (FM) sweeps is an important temporal cue in animal and human communication. FM direction-selective neurons are found in the primary auditory cortex (A1), but their topography and the mechanisms underlying their selectivity remain largely unknown. Here we report that in the rat A1, direction selectivity is topographically ordered in parallel with characteristic frequency (CF): low CF neurons preferred upward sweeps, whereas high CF neurons preferred downward sweeps. The asymmetry of 'inhibitory sidebands', suppressive regions flanking the tonal receptive field (TRF) of the spike response, also co-varied with CF. In vivo whole-cell recordings showed that the direction selectivity already present in the synaptic inputs was enhanced by cortical synaptic inhibition, which suppressed the synaptic excitation of the non-preferred direction more than that of the preferred. The excitatory and inhibitory synaptic TRFs had identical spectral tuning, but with inhibition delayed relative to excitation. The spectral asymmetry of the synaptic TRFs co-varied with CF, as had direction selectivity and sideband asymmetry, and thus suggested a synaptic mechanism for the shaping of FM direction selectivity and its topographic ordering.

Acoustic Stimulation↗
PubMed2005

Hearing loss raises excitability in the auditory cortex.

Developmental hearing impairments compromise sound discrimination, speech acquisition, and cognitive function; however, the adjustments of functional properties in the primary auditory cortex (A1) remain unknown. We induced sensorineural hearing loss (SNHL) in developing gerbils and then reared the animals for several days. The intrinsic membrane and synaptic properties of layer 2/3 pyramidal neurons were subsequently examined in a thalamocortical brain slice preparation with whole-cell recordings and electron microscopic immunocytochemistry. SNHL neurons displayed a depolarized resting membrane potential, an increased input resistance, and a higher incidence of sustained firing. They also exhibited significantly larger thalamocortically and intracortically evoked excitatory synaptic responses, including a greater susceptibility to the NMDA receptor antagonist AP-5 and the NR2B subunit antagonist ifenprodil. This correlated with an increase in NR2B labeling of asymmetric synapses, as visualized ultrastructurally. Furthermore, decreased frequency and increased amplitude of miniature EPSCs (mEPSCs) in SNHL neurons suggest that a decline in presynaptic release properties is compensated by an increased excitatory response. To verify that the increased thalamocortical excitation was elicited by putative monosynaptic connections, minimum amplitude ventral medial geniculate nucleus-evoked EPSCs were recorded. These minimum-evoked responses were of larger amplitude, and the NMDAergic currents were also larger and longer in SNHL neurons. These findings were supported by significantly longer AP-5-sensitive durations and larger amplitudes of mEPSCs. Last, the amplitudes of intracortically evoked monosynaptic and polysynaptic GABAergic inhibitory synaptic responses were significantly smaller in SNHL neurons. These alterations in cellular properties after deafness reflect an attempt by A1 to sustain an operative level of cortical excitability that may involve homeostatic mechanisms.

Adaptation, Physiological↗
PubMed1998

Click train encoding in primary auditory cortex of the awake monkey: evidence for two mechanisms subserving pitch perception.

Multiunit activity (MUA) and current source density (CSD) patterns evoked by click trains are examined in primary auditory cortex (A1) of three awake monkeys. Temporal and spectral features of click trains are differentially encoded in A1. Encoding of temporal features occurs at rates of 100-200 Hz through phase-locked activity in the MUA and CSD, is independent of pulse polarity pattern, and occurs in high best frequency (BF) regions of A1. The upper limit of ensemble-wide phase-locking is about 400 Hz in the input to A1, as manifested in the cortical middle laminae CSD and MUA of thalamocortical fibers. In contrast, encoding of spectral features occurs in low BF regions, and resolves both the f0 and harmonics of the stimuli through local maxima of activity determined by the tonotopic organization of the recording sites. High-pass filtered click trains decrease spectral encoding in low BF regions without modifying phase-locked responses in high BF regions. These physiological responses parallel features of human pitch perception for click trains, and support the existence of two distinct physiological mechanisms involved in pitch perception: the first using resolved harmonic components and the second utilizing unresolved harmonics that is based on encoding stimulus waveform periodicity.

Animals↗
PubMed2003

Binaural interaction in the human auditory cortex revealed by neuromagnetic frequency tagging: no effect of stimulus intensity.

Frequency tagging of magnetoencephalographic signals was recently introduced as a new tool to study binaural interaction in the human auditory cortex [Fujiki et al., J. Neurosci. 22 (2002) RC205]. As the method has potential value for assessing brain plasticity in patients with unilateral hearing deficits, we studied binaural interaction in 10 healthy adults at different intensity levels. Cortical steady-state fields were measured with a 306-channel whole-scalp neuromagnetometer to amplitude-modulated sounds (carrier frequency 1 kHz), presented monaurally or binaurally at 45, 60 and 75 dB SL. The modulation frequencies were 39.1 Hz for the right ear and 41.1 Hz for the left. During binaural stimulation, the ipsilateral responses were suppressed more than the contralateral ones in both hemispheres, and the hemispheric balance shifted towards the contralateral hemisphere for inputs from both ears. The patterns of binaural interaction were similar at all three stimulus intensities. These data could be useful in examining patients who suffer from auditory disorders as well as in revealing basic mechanism of human auditory processing.

Acoustic Stimulation↗