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Effects of noise-induced hearing loss at young age on voice onset time and gap-in-noise representations in adult cat primary auditory cortex.

Here we show that mild hearing loss induced by noise exposure in early age causes a decrease in neural temporal resolution when measured in adulthood. We investigated the effect of this chronic hearing loss on the representation of a voice onset time (VOT) and a gap-duration continuum in primary auditory cortex (AI) in cats, which were exposed at the age of 6 weeks to a 120-dB SPL, 5-kHz 1/3 octave noise band for 2 h. The resulting hearing loss measured using auditory brainstem responses and cortical multiunit thresholds at 4-6 months of age was 20-40 dB between 1 and 32 kHz. Multiple single-unit activity was recorded in seven noise-exposed cats and nine control cats related to the presentation of a/ba/-/pa/ continuum in which VOT was varied in 5-ms step from 0 to 70 ms. We also obtained data for noise bursts with gaps, of duration equal to the VOT, embedded in noise 5 ms after the onset. Both stimuli were presented at 65 dB SPL. Minimum VOT and early-gap duration were defined as the lowest value in which an on-response, significantly above the spontaneous activity, to both the leading and trailing noise bursts or vowel was obtained. The mild chronic noise-induced hearing loss increased the minimum detectable VOT and gap duration by 10 ms. We also analyzed the maximum firing rate (FRmax) and the latency of the responses as a function of VOT and gap duration and found a significant reduction in the FRmax to the trailing noise burst for gap durations above 50 ms. This suggests that mild hearing loss acquired in early age may affect cortical temporal processing in adulthood.

Acoustic Stimulation↗

Temporal response features of cat auditory cortex neurons contributing to sensitivity to tones delivered in the presence of continuous noise.

Single cat auditory cortex neurons have limited intensity dynamic ranges for characteristic frequency (CF) tones. In the presence of continuous wide-spectrum noise, these cells' tone responses undergo a dynamic range shift towards higher SPLs. In the present study, the mechanisms underlying this dynamic range shift were examined by probing the sensitivity of the cells to CF tones delivered at various delays after the onset and/or offset of a long duration noise mask. Fifty cells were studied in the cortex of 7 anesthetized cats using acoustically mixed tonal and noise stimuli presented monaurally to the contralateral ear through a calibrated, sealed stimulating system. For most neurons, the dynamic range shift induced by continuous noise was fully developed in the responses to CF tones delivered 100-250 ms after the onset of a noise mask. For nonmonotonic cells, shorter delays between noise and tone onsets resulted in a profound suppression of tone responses that was consistent with the view that noise stimuli evoke a short latency, but transient, inhibitory response in these neurons. Studies of monotonic cells with short tone delays revealed that the usual excitatory response to noise onset was sometimes followed by a period of inhibition. In most cells, as soon after mask onset that CF tones were able to evoke spike discharges, those responses had latent periods comparable to those of responses to tones of the same SPL delivered in continuous noise. After the offset of an 800 ms noise mask effecting a 15-25 dB dynamic range shift for CF tones, recovery of tone sensitivity to within 5 dB of control levels typically took 50-200 ms. On the basis of these observations, it is argued that in order for a CF tone to excite a cortical neuron after the onset of a noise mask, the tone amplitude must be sufficient to overcome both the transient central neural consequences of noise onset, and a short-term adaptation that is probably peripheral in origin. The implications of these data for the sensitivity of cortical cells to temporally varying stimuli are discussed.

Animals↗

Phase-locked responses to pure tones in the primary auditory cortex.

At the level of the brainstem, precise temporal information is essential for some aspects of binaural processing, while at the level of the cortex, rate and place mechanisms for neural coding seem to predominate. However, we now show that precise timing of steady-state responses to pure tones occurs in the primary auditory cortex (AI). Recordings were made from 163 multi-units in guinea pig AI. All units increased their firing rate in response to pure tones at 100 Hz and 46 (28%) gave sustained responses which were synchronised with the stimulus waveform (phase-locking). The phase-locking units were clustered together in columns. Phase-locking was generally strongest in layers III and IV but was also recorded in layers I, II and V. Good phase-locking was observed over a range of 60-250 Hz: some units (30%) were narrow band while others (37%) were low-pass (33% were not determined). Phase-locking strength was also influenced by sound level: some units showed monotonic increases in strength with level and others were non-monotonic. Ten of the units provided a good temporal representation of the fundamental frequency (270 Hz) of a guinea pig vocalisation (rumble) and may be involved in analysing communication calls.

Acoustic Stimulation↗

Timing and laminar profile of eye-position effects on auditory responses in primate auditory cortex.

We examined effects of eye position on auditory cortical responses in macaques. Laminar current-source density (CSD) and multiunit activity (MUA) profiles were sampled with linear array multielectrodes. Eye position significantly modulated auditory-evoked CSD amplitude in 24/29 penetrations (83%), across A1 and belt regions; 4/24 cases also showed significant MUA AM. Eye-position effects occurred mainly in the supragranular laminae and lagged the co-located auditory response by, on average, 38 ms. Effects in A1 and belt regions were indistinguishable in amplitude, laminar profile, and latency. The timing and laminar profile of the eye-position effects suggest that they are not combined with auditory signals at a subcortical stage of the lemniscal auditory pathways and simply "fed-forward" into cortex. Rather, these effects may be conveyed to auditory cortex by feedback projections from parietal or frontal cortices, or alternatively, they may be conveyed by nonclassical feedforward projections through auditory koniocellular (calbindin positive) neurons.

Acoustic Stimulation↗

Electrophysiological mapping of cat primary auditory cortex with multielectrode arrays.

The present study employs simultaneous multielectrode recording techniques to study the feline primary auditory cortex (AI) to characterize its functional architecture. High electrode-count microelectrode arrays provide a high spatial and temporal view of AI, but at the potential cost of significant cortical insult. However, the number of electrodes that record single- and multiunit action potentials shown in this study suggest that the implantation of high electrode-count microelectrode arrays allows for reliable recordings from the cortex and that the neurons abutting the electrode tips appear to be spared from significant insult. Using these recordings, we have constructed a functional model of AI that best specifies the distribution of characteristic frequencies (CF's), and have reaffirmed that CF is logarithmically distributed across the cortical surface with a principal CF axis perpendicular to generally straight isofrequency contours. In four cats, we found that the average CF gradient was 0.53 +/- 0.08 octave per millimeter. This study demonstrates the use of high electrode count, microelectrode array recordings in characterizing the spatial distribution of acoustic information in the feline AI.

Acoustic Stimulation↗

Learning-induced dynamic receptive field changes in primary auditory cortex of the unanaesthetized Mongolian gerbil.

Learning-induced changes of the spectro-temporal characteristics of primary auditory cortex (AI) units were studied by response plane analysis of recordings from the AI in unanaesthetized Mongolian gerbils. Using response planes obtained prior to and after auditory discrimination training bins of significant change were identified and their spectro-temporal distribution was studied. Bins of significant changes were generally found to be distributed over the entire spectro-temporal receptive field but occurred most frequently within the first 100 ms of response in the spectral neighbourhood (1.5 octaves) of the frequency of the reinforced conditioned stimulus. Training-induced response decreases occurred early after 10 ms for reinforced conditioned tones and tones in the frequency neighbourhood. Response increases occurred so early only for non-reinforced tones in the neighbourhood of the reinforced frequency and occurred later (after 40 ms) for the reinforced tones. The results are discussed in the light of dynamic disinhibition.

Animals↗

Lateral inhibition in the auditory cortex: an EEG index of tinnitus?

Auditory ERPs were recorded from eight tinnitus patients and 12 controls. Tone pips of 1000 and 2000 Hz, as well as the patient's tinnitus pitch (around 4000 Hz) were used. Controls received tone pips at 1000, 2000, and 4000 Hz. Tones were presented at 30, 36, 42, 48 and 54 dB/SL. The intensity dependence of the auditory N100 was calculated for each frequency in each group. Patients showed a steeper response to the tinnitus frequency than responses to the 4000 Hz tone in controls. In contrast, intensity-dependence to the 2000 Hz tones was significantly decreased in patients (two-tailed Wilcoxon-Mann-Whitney U-test, p < 0.05). Responses to the 1000 Hz tones were similar for both groups. This reduced intensity dependence is hypothesized to result from lateral inhibition arising from tinnitus related activity in the 4000 Hz isofrequency region.

Acoustic Stimulation↗

Functional organization of squirrel monkey primary auditory cortex: responses to frequency-modulation sweeps.

The squirrel monkey twitter call is an exemplar of a broad class of species-specific vocalizations that contain naturally voiced frequency-modulated (FM) sweeps. To investigate how this prominent communication call element is represented in primary auditory cortex (AI), neuronal receptive field properties to pure-tone and synthetic, logarithmically spaced FM-sweep stimuli in 3 barbiturate-anesthetized squirrel monkeys are studied. Responses to pure tones are assessed by using standard measures of frequency response areas, whereas responses to FM sweeps are classified according to direction selectivity, best speed, and speed tuning preferences. Most neuronal clusters respond to FM sweeps in both directions and over a range of FM speeds. Center frequencies calculated from the average of high and low trigger frequency edges of FM response profiles are highly correlated with pure-tone characteristic frequencies (CFs). However, bandwidth estimates are only weakly correlated with their pure-tone counterparts. CF and direction selectivity are negatively correlated. Best speed maps reveal idiosyncratically positioned spatial aggregation of similar values. In contrast, direction selectivity maps show unambiguous spatial organization. Neuronal clusters selective for upward-directed FM sweeps are located in ventral-caudal AI, where CFs range from 0.5 to 1 kHz. Combinations of pure-tone and FM response parameters form 2 significant factors to account for response variations. These results are interpreted in the context of earlier FM investigations and neuronal encoding of dynamic sounds.

Acoustic Stimulation↗

Representation of the cochlea in primary auditory cortex of the ferret (Mustela putorius).

In seven barbiturate-anesthetized ferrets, we explored the acoustically sensitive cortex with conventional microelectrode mapping techniques. A tonotopically organized field was found whose orientation was such that high tonal frequencies were represented dorsally, and low frequencies ventrally. Within this field, neurons typically had short (12-20 ms) latent periods to first spikes. In conjunction with extant anatomical evidence on the connectivity of this region, these data suggest that this field represents the ferret's primary auditory cortex.

Animals↗

Modulation of level response areas and stimulus selectivity of neurons in cat primary auditory cortex.

Sounds commonly occur in sequences, such as in speech. It is therefore important to understand how the occurrence of one sound affects the response to a subsequent sound. We approached this question by determining how a conditioning stimulus alters the response areas of single neurons in the primary auditory cortex (AI) of barbiturate-anesthetized cats. The response areas consisted of responses to stimuli that varied in level at the two ears and delivered at the characteristic frequency of each cell. A binaural conditioning stimulus was then presented > or =50 ms before each of the stimuli comprising the level response area. An effective preceding stimulus alters the shape and severely reduces the size and response magnitude of the level response area. This ability of the preceding stimulus depends on its proximity in the level domain to the level response area, not on its absolute level or on the size of the response it evokes. Preceding stimuli evoke a nonlinear inhibition across the level response area that results in an increased selectivity of a cortical neuron for its preferred binaural stimuli. The selectivity of AI neurons during the processing of a stream of acoustic stimuli is likely to be restricted to a portion of their level response areas apparent in the tone-alone condition. Thus rather than being static, level response areas are fluid; they can vary greatly in extent, shape and response magnitude. The dynamic modulation of the level response area and level selectivity of AI neurons might be related to several tasks confronting the central auditory system.

Acoustic Stimulation↗

Coding of tone-pulse amplitude by single neurons in auditory cortex of albino rats (Rattus norvegicus).

We examined the neural representation of tone pulse amplitude in the auditory cortex of anesthetized albino rats. Rate-level functions for monaural, contralateral CF tones were obtained from single neurons. Most of these functions were saturating and monotonic in shape. The dynamic ranges of these functions were typically 5 to 35 dB in breadth, although the tail of this distribution extended to beyond 60 dB. The neurons with the widest dynamic ranges were usually those with the lowest CF thresholds. Nonmonotonic neurons were uncommon, and the nonmonotonicity was not as well developed as that seen in the cortex of cats and monkeys. For two individual rats, data are presented for neurons tuned to the same tone frequency in a single cerebral hemisphere. The CF thresholds of these neurons varied over a 50 dB range, and their collective dynamic ranges spanned at least 70 dB. These data provide a minimum estimate of the dynamic range of the cortical code for tone pulse amplitude in the rat. They suggest that there may be no serious mismatch between the neural and behavioral amplitude dynamic ranges.

Acoustic Stimulation↗

Different modes of pitch perception and learning-induced neuronal plasticity of the human auditory cortex.

We designed a melody perception experiment involving eight harmonic complex tones of missing fundamental frequencies (hidden auditory object) to study the short-term neuronal plasticity of the auditory cortex. In this experiment, the fundamental frequencies of the complex tones followed the beginning of the virtual melody of the tune "Frère Jacques". The harmonics of the complex tones were chosen so that the spectral melody had an inverse contour when compared with the virtual one. Evoked magnetic fields were recorded contralaterally to the ear of stimulation from both hemispheres. After a base line measurement, the subjects were exposed repeatedly to the experimental stimuli for 1 hour a day. All subjects reported a sudden change in the perceived melody, indicating possible reorganization of the cortical processes involved in the virtual pitch formation. After this switch in perception, a second measurement was performed. Cortical sources of the evoked gamma-band activity were significantly stronger and located more medially after a switch in perception. Independent Component Analysis revealed enhanced synchronization in the gamma-band frequency range. Comparing the gamma-band activation of both hemispheres, no laterality effects were observed. The results indicate that the primary auditory cortices are involved in the process of virtual pitch perception and that their function is modifiable by laboratory manipulation.

Adult↗

The dual pattern of corticothalamic projection of the primary auditory cortex in macaque monkey.

The distribution and terminal morphology of the corticothalamic projection originating from the primary auditory cortex (A1) were established in a macaque monkey, using the anterograde (and retrograde) tracer biotinylated dextran amine. A dense corticothalamic projection from A1 was found in the ventral (vMGB) and dorsal (dMGB) divisions of the medial geniculate body and, to a lesser extent, in the medial division (mMGB), the posterior thalamic nucleus (PO) and the suprageniculate nucleus. Most terminal boutons were small (<1 microm), except some large boutons (2-6 microm) located in PO and vMGB. The data demonstrate that the corticothalamic projection from A1 in primate consists of two types of terminals (small and giant endings) in line with previous observations in rat and cat. Retrogradely labeled thalamocortical neurons formed clusters generally overlapping the corticothalamic terminal fields.

Animals↗

Binaural and frequency representation in the primary auditory cortex of the big brown bat, Eptesicus fuscus.

This study examines the binaural and frequency representation in the primary auditory cortex (AC) of the big brown bat, Eptesicus fuscus, by using an ear-phone stimulation system. All 306 cortical neurons studied were excited by contralateral sound stimulation but they were either excited, inhibited or not affected by ipsilateral sound stimulation. These cortical neurons were columnarly organized according to their binaural and frequency-tuning properties. The excitation-excitation columns which occupy about 15% of the AC are mainly aggregated within an oval-shaped area of the central AC. The excitation-inhibition neurons and binaural neurons with mixed properties are distributed in the remaining 85% of the surrounding primary AC. Although the best frequency (BF) of these neurons shows a tendency to decrease from high to low along the anteroposterior axis of the primary AC, systematic variation in BF is not always consistent across the entire mapping area. In particular, BFs of cortical neurons isolated in the anterior AC vary quite unsystematically such that neurons with similar BFs are aggregated in isolated patches. Isofrequency and binaural columns are segregated into bands that intersect each other.

Acoustic Stimulation↗

Temporal firing patterns of single units, pairs and triplets of units in the auditory cortex.

The spontaneous and acoustically driven activities of single units, pairs and triplets of units in the auditory cortex were analyzed. Data were obtained in two sets of experiments from nonbehaving awake cats and from a behaving monkey. The results of the two sets of experiments indicated that neighboring neurons usually fire independently. The weak correlations found between pairs of adjacent neurons were mostly indicative of a common input driving both units. In some cases, signs of synaptic interaction between the neurons were found. When triplets of units were considered, it was found that several independent inputs exist, even within a small group of adjacent neurons. When such small groups of neurons were studied in the behaving monkey, it was found that the temporal firing pattern of single neurons and the interactions between pairs of neurons were in some cases dependent on the behavioral state and on the sensorimotor association.

Animals↗

Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. II. Auditory cortex plasticity.

The 2-deoxyglucose (2-DG) method was used to map the metabolic activity of the auditory cortex (AC) during and after conditioning. Using separate groups of animals, the effects of both paired and unpaired presentations of a 4-5 kHz FM tone (CS) and midbrain reticular stimulation (US) were compared for acquisition, extinction and sensitization training. Rats with cardiac deceleration conditioned to the FM tone showed a pattern of AC metabolic activity distinctly different from that seen in control animals. The tonotopic pattern of 2-DG labeling consisted of two contiguous spindle-shaped bands corresponding to the location of neurons with best frequency response in the 4-5 kHz band width. Reticular stimulation alone or combined with the tones produced a widespread increase of 2-DG uptake. At least two types of modulatory effects appeared to interact with the tonotopic pattern. The first involved a selective enhancement of evoked activity in the AC region of convergence of CS-US effects. This effect may be related to learning because it was restricted to the conditioning group. The second effect involved a general increase in background uptake of 2-DG in AC. This effect may be related to reticular sensitization because it was common to all groups subjected to reticular stimulation. The present findings are the first anatomical demonstration of the modulatory effects of auditory learning on AC metabolic activity.

Animals↗