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Physiological plasticity of single neurons in auditory cortex of the cat during acquisition of the pupillary conditioned response: II. Secondary field (AII).

The discharges of 22 single neurons were recorded in the secondary auditory cortical field (AII) during acquisition of the pupillary dilation conditioned defensive response in chronically prepared cats. All 22 neurons developed discharge plasticity in background activity, and 21/22 cells developed plasticity in their responses to the acoustic conditioned stimulus (CS). Nonassociative factors were ruled out by the use of a sensitization phase (CS and US [unconditioned stimulus] unpaired) preceding the conditioning phase and by ensuring stimulus constancy at the periphery by neuromuscular paralysis. Changes in background neuronal activity were related to measures of behavioral learning or to changes in the level of arousal. Specifically, decreases in background activity (17/22 cells) developed at the time that subjects began to display conditioned responses. Increases in background activity (5/22) developed in animals that became more tonically aroused during conditioning. However, both increases (11/22) and decreases (10/22) in evoked activity developed independently of the rate of pupillary learning, tonic arousal level, or changes in background activity. These findings indicate that changes in background activity are closely related to behavioral processes of learning and arousal whereas stimulus-evoked discharge plasticity develops solely as a consequence of stimulus pairing. A comparative analysis of the effects of conditioning on secondary and primary (AI) auditory cortex indicates that both regions develop neuronal discharge plasticity early in the conditioning phase and that increases in background activity in primary auditory cortex are also associated with elevated levels of tonic arousal. In addition, the overall incidence of single neurons developing learning-related discharge plasticity is significantly greater in AII than in AI. The relevance of these findings is discussed in terms of parallel processing in sensory systems and multiple sensory cortical fields.

Animals↗

fMRI studies of sensitivity and habituation effects within the auditory cortex at 1.5 T and 3 T.

PURPOSE: To assess habituation effects in relation to field strength by fMRI at 1.5 vs. 3.0 T within the auditory cortex of healthy subjects. MATERIALS AND METHODS: fMRI experiments were performed on 19 healthy subjects at 1.5 T (N = 12) and 3 T (N = 12). The auditory cortex was stimulated binaurally by digitally generated pulsed (nu = 5 Hz) 800 Hz sine tones with three alternating on and off periods. RESULTS: The mean activation after stimulation (4.4% +/- 1.2% (1.5 T) and 5.3% +/- 2.3% (3 T)) and number of activated pixels (96.7 +/- 49.8 (1.5 T) and 139.9 +/- 101 (3 T)) were higher at 3 T compared to 1.5 T; however, that difference did not reach statistical significance. A characteristic signal decay with repeated stimuli was revealed at both 1.5 and 3 T, and the response to the second and third stimulation blocks was significantly lower compared to the first. The habituation pattern was the same, independently of field strength and age. CONCLUSION: The mean activation and number of pixels were only modestly higher at 3 T, probably due to higher physiologic noise and higher local macroscopic susceptibility gradients within the temporal lobes at 3 T. Our data reveal that measured auditory habituation is independent of field strength, and data obtained at two different field strengths do not differ fundamentally in this context.

Acoustic Stimulation↗

Memory consolidation for the discrimination of frequency-modulated tones in mongolian gerbils is sensitive to protein-synthesis inhibitors applied to the auditory cortex.

Differential conditioning of Mongolian gerbils to linearly frequency-modulated tones (FM) has recently received experimental attention. In the study of the role of cerebral protein synthesis for FM discrimination memory, gerbils received post-training bilateral injections of anisomycin into the auditory cortex under light halothane anesthesia. Compared with saline-treated controls, anisomycin-treated gerbils showed a discrimination decrement during the subsequent three days of training. They markedly improved their performance within training sessions, but started each session at low levels. When repeatedly trained gerbils received post-session injections of anisomycin, discrimination performance during subsequent sessions was similar to the pre-injection performance, indicating that retention, retrieval, reconsolidation, and expression of the established reaction were not affected. However, the improvement of a partially established discrimination reaction was impaired after this treatment. Intracortical injections of emetine confirmed this finding. Neither drug affected FM discrimination learning when given several days before the initial training. Our results suggest that protein-synthesis inhibitors applied to the auditory cortex of gerbils during the post-acquisition phase interfered with learning and memory-related aspects of FM processing. The resulting deficit was evident for a number of post-injection training days. This effect was probably due to impaired consolidation, i.e., processes required for long-term stabilization or retrieval of the memory trace while leaving short-term memory intact.

Acoustic Stimulation↗

[Ultrastructural organization of projection zones AI and AIV of the cat auditory cortex to the inferior colliculi].

By the method of anterograde degeneration, distribution of projections of functionally definite AI and AIV zones of the cat auditory cortex have been studied in the posterior calculi of the tectum opticum. It has been demonstrated electron microscopically that an essentially part of the degenerating boutons are found in the middle and caudal thirds of the colliculi, and the remaining ones terminate on the dendrites with large- and middle-size diameters and on the spines. A supposition is made that there exist two systems of the corticofugal auditory fibres. Peculiarities of the degenerative rates, specific for short- and long-axonal systems of the fibres and possible mechanisms for the influence of the auditory cortex on the neurons of the posterior colliculi of the tectum opticum are discussed.

Animals↗

Magnetoencephalographic 10-Hz rhythm from the human auditory cortex.

Spontaneous magnetoencephalographic activity was recorded with a 24-SQUID gradiometer over the lateral aspects of the head in 3 healthy adults. All subjects displayed 8-10 Hz rhythmic activity which was not affected by opening of the eyes but was occasionally dampened by auditory stimuli. The equivalent sources of the rhythm were in the supratemporal auditory cortex, and the activity may therefore represent 'idling' of the auditory cortex. Obviously each sensory projection cortex has its own local spontaneous rhythm.

Acoustic Stimulation↗

Morphology and laminar distribution of nonpyramidal neurons in the auditory cortex of the rabbit.

A study of the morphology and laminar distribution of nonpyramidal neurons in Golgi-Nissl preparations of electrophysiologically verified auditory cortex was carried out in the adult rabbit. Nonpyramidal neurons were located primarily within laminae I-IV and were only infrequently seen in lamina V and VI. In lamina I, four nonpyramidal cell types were observed: (1) small, spine-free horizontal neurons, (2) small, sparsely spined multipolar neurons with radiate dendrites, (3) large, multipolar neurons with fusiform somata and vertically aligned, sparsely spined dendrites, and (4) small, spine-free neurogliform neurons. The horizontal and small multipolar neurons had tangentially running axons confined to lamina I. The large, fusiform cells had descending axons which arborized in lamina II and occasionally reached lamina III. In lamina II and the upper part of lamina III, seven nonpyramidal cell types were observed: (1) spine-free bipolar neurons with vertically aligned dendrites and axonal arbors; (2) large, (3) medium, and (4) small, spine-free and sparsely spined multipolar neurons, all with locally ramifying axons; (5) pear-shaped cells with highly oriented dendrites which branched toward the pial surface and vertically arborizing axons; (6) multipolar cells with tangentially and vertically oriented dendrites and ascending axons which entered lamina I, and (7) tufted cells with local axons. Three types of nonpyramidal cells were observed in lamina IV and the lower part of lamina III: (1) large, multipolar cells with radiate, spine-free dendrites and stout axons which arborized locally, (2) spiny multipolar cells with vertically aligned dendrites and ascending axons which arborized in lamina II and III via long horizontal collaterals, and (3) spine-free bipolar cells with vertical dendrites and axons which arborized in a narrow vertical column adjacent to the dendrites. Nonpyramidal neurons in lamina V and VI were primarily multipolar cells with sparsely spined and spine-free dendrites. A comparison of these data with those of other species indicates that the neuronal organization of the rabbit auditory cortex is similar to that of the sensory cortex of the rodent but is strikingly different from that of carnivores and primates.

Animals↗

Intracerebral evoked potentials in pitch perception reveal a functional asymmetry of the human auditory cortex.

One acoustic feature that plays an important role in pitch perception is frequency. Studies on the processing of frequency in the human and animal brain have shown that the auditory cortex is tonotopically organized: low frequencies are represented laterally whereas high frequencies are represented medially. To date, the study of the functional organization of the human auditory cortex in the processing of frequency has been limited to the use of either scalp-recorded auditory evoked potentials (AEPs), which have relatively poor spatial resolving power, or functional imagery techniques, which have poor temporal resolving power. The present study uses intracerebrally recorded AEPs to explore this topic in the primary and secondary auditory cortices of both hemispheres of the human brain. Recordings were carried out in 45 adult patients with drug-resistant partial seizures. In the right hemisphere, clear spectrally organized tonotopic maps were observed with distinct separations between different frequency-processing regions. AEPs for high frequencies were recorded medially, whereas AEPs for low frequencies were recorded laterally. In the left hemisphere, however, this tonotopic organization was less evident, with different regions involved in the processing of a range of frequencies. The hemisphere-related difference in the processing of tonal frequency is discussed in relation to pitch perception.

Acoustic Stimulation↗

Temporal encoding of the voice onset time phonetic parameter by field potentials recorded directly from human auditory cortex.

Voice onset time (VOT) is an important parameter of speech that denotes the time interval between consonant onset and the onset of low-frequency periodicity generated by rhythmic vocal cord vibration. Voiced stop consonants (/b/, /g/, and /d/) in syllable initial position are characterized by short VOTs, whereas unvoiced stop consonants (/p/, /k/, and t/) contain prolonged VOTs. As the VOT is increased in incremental steps, perception rapidly changes from a voiced stop consonant to an unvoiced consonant at an interval of 20-40 ms. This abrupt change in consonant identification is an example of categorical speech perception and is a central feature of phonetic discrimination. This study tested the hypothesis that VOT is represented within auditory cortex by transient responses time-locked to consonant and voicing onset. Auditory evoked potentials (AEPs) elicited by stop consonant-vowel (CV) syllables were recorded directly from Heschl's gyrus, the planum temporale, and the superior temporal gyrus in three patients undergoing evaluation for surgical remediation of medically intractable epilepsy. Voiced CV syllables elicited a triphasic sequence of field potentials within Heschl's gyrus. AEPs evoked by unvoiced CV syllables contained additional response components time-locked to voicing onset. Syllables with a VOT of 40, 60, or 80 ms evoked components time-locked to consonant release and voicing onset. In contrast, the syllable with a VOT of 20 ms evoked a markedly diminished response to voicing onset and elicited an AEP very similar in morphology to that evoked by the syllable with a 0-ms VOT. Similar response features were observed in the AEPs evoked by click trains. In this case, there was a marked decrease in amplitude of the transient response to the second click in trains with interpulse intervals of 20-25 ms. Speech-evoked AEPs recorded from the posterior superior temporal gyrus lateral to Heschl's gyrus displayed comparable response features, whereas field potentials recorded from three locations in the planum temporale did not contain components time-locked to voicing onset. This study demonstrates that VOT at least partially is represented in primary and specific secondary auditory cortical fields by synchronized activity time-locked to consonant release and voicing onset. Furthermore, AEPs exhibit features that may facilitate categorical perception of stop consonants, and these response patterns appear to be based on temporal processing limitations within auditory cortex. Demonstrations of similar speech-evoked response patterns in animals support a role for these experimental models in clarifying selected features of speech encoding.

Auditory Cortex↗

Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey.

Recent experiments in the cat have demonstrated that several response parameters, including frequency tuning, intensity tuning, and FM selectivity, are spatially segregated across the isofrequency axis. To investigate whether a similar functional organization exists in the primate, we have studied the spatial distribution of pure-tone receptive field parameters across the primary auditory cortex (AI) in six owl monkeys (Aotus trivirgatus). The distributions of binaural interaction types and onset latency were also examined. Consistent with previous studies, the primary auditory cortex contained a clear cochleotopic organization. We demonstrate here that several other properties of the responses to tonal stimuli also showed nonrandom spatial distributions that were largely independent from each other. In particular, the sharpness of frequency tuning to pure tones, intensity tuning and sensitivity, response latency, and binaural interaction types all showed spatial variations that were independent from the representation of characteristic frequency and from each other. Statistical analysis confirmed that these organizations did not reflect random distributions. The overall organizational pattern of overlaying but independent functional maps that emerged was quite similar to that seen in AI of cats and, in general, appears to reflect a fundamental organization principle of primary sensory cortical fields.

Action Potentials↗

Interaction between excitation and inhibition affects frequency tuning curve, response size and latency of neurons in the auditory cortex of the big brown bat, Eptesicus fuscus.

Neurons in the auditory cortex (AC) receive convergent excitatory and inhibitory inputs from the lower auditory nuclei. Interaction between these two opposing inputs shapes different response properties of AC neurons. In this study, we examined how this interaction might affect the frequency tuning curves (FTCs), number of impulses and latency of AC neurons in the big brown bat, Eptesicus fuscus, using a probe (excitatory tone) and a masker (inhibitory tone) under different stimulation conditions. Excitatory FTCs of AC neurons were either V-shaped, closed (i.e. upper threshold) or double-peaked. Inhibitory FTCs were obtained either at both flanks or only at the low or high flank of excitatory FTCs. Application of bicuculline, an antagonist for gamma-aminobutyric acid A receptors, produced expansion of excitatory FTCs into predrug inhibitory FTCs. Inhibition of probe-elicited responses occurred when a masker was presented at certain intertone intervals. Maximal inhibition typically took place when a masker was presented within 4 ms prior to the probe. During maximal inhibition, a neuron had the minimal number of impulses and the longest response latency. Inhibition became stronger with increasing masker intensity but became weaker with increasing intertone interval. Biological significance of these data is discussed.

Acoustic Stimulation↗

The processing of temporal pitch and melody information in auditory cortex.

An fMRI experiment was performed to identify the main stages of melody processing in the auditory pathway. Spectrally matched sounds that produce no pitch, fixed pitch, or melody were all found to activate Heschl's gyrus (HG) and planum temporale (PT). Within this region, sounds with pitch produced more activation than those without pitch only in the lateral half of HG. When the pitch was varied to produce a melody, there was activation in regions beyond HG and PT, specifically in the superior temporal gyrus (STG) and planum polare (PP). The results support the view that there is hierarchy of pitch processing in which the center of activity moves anterolaterally away from primary auditory cortex as the processing of melodic sounds proceeds.

Acoustic Stimulation↗

The impact of auditory cortex activity on characterizing and treating patients with chronic tinnitus--first results from a PET study.

CONCLUSION: Unilaterally increased metabolic activity within the primary auditory cortex (PAC) represents a robust finding in tinnitus patients. Targeting these hyperactive areas with image-guided low frequency repetitive transcranial magnetic stimulation (rTMS) results in subjective tinnitus reduction. More pronounced activation of the PAC predicted higher resistance to rTMS. OBJECTIVES: [18F]deoxyglucose (FDG)-positron emission tomography (PET) was used to assess metabolic activity within the central auditory system in tinnitus. The study investigated whether patterns of neuronal activity correlate with clinical features or may be used for the prediction of treatment outcome. PATIENTS AND METHODS: Twenty patients with chronic tinnitus underwent PET imaging followed by low frequency rTMS treatment. Neuroimaging data were compared with clinical parameters and treatment outcome. RESULTS: PET data demonstrated an asymmetric activation of the central auditory system. Seventeen patients revealed increased activity of the primary auditory cortex on the left side, three on the right side. The extent of hypermetabolic activity prior to treatment correlated significantly with tinnitus reduction after rTMS, but not with clinical characteristics such as tinnitus severity, tinnitus laterality or tinnitus duration.

Adult↗

Differences in response properties of neurons between two delay-tuned areas in the auditory cortex of the mustached bat.

1. The orientation sound (pulse) of the mustached bat, Pteronotus parnellii parnellii, consists of four harmonics (H1-4), each containing a long constant-frequency component (CF1-4) followed by a short frequency-modulated component (FM1-4). The auditory cortex of this species contains several "combination-sensitive" areas: FM-FM, dorsal fringe (DF), ventral fringe (VF), CF/CF, and H1-H2. The FM-FM, DF, and VF areas each consist of neurons tuned to particular delays of echo FMn (n = 2, 3, or 4) from pulse FM1, and have an echo-delay (target-range) axis. This delay axis is from 0.4 to approximately 18 ms in the FM-FM area, to approximately 9 ms in the DF area, and to approximately 5 ms in the VF area. Therefore we hypothesized that the VF area was more specialized for the processing of range information in the terminal phase of echolocation than was the FM-FM area. The aim of our present studies was to find differences in response properties between neurons with best delays shorter than 6 ms in the VF and FM-FM areas and thus to test our hypothesis. 2. In the terminal phase of target-directed flight, the rate of pulse emission becomes higher, pulse duration (in particular, CF duration) becomes shorter, echo delay becomes shorter, and echoes (both the CF and FM components) are less Doppler shifted. Therefore, a "temporal-pattern-simulating (TPS)" stimulus was designed to mimic the train of pulse-echo pairs that would be heard by the bat during the terminal phase, and responses of single neurons to the TPS stimulus and other types of stimuli were recorded from the VF and FM-FM areas of the auditory cortex of unanesthetized bats with a tungsten-wire microelectrode. 3. Best delays of the neurons studied range between 0.9 and 5.5 ms (2.64 +/- 0.72 ms, N = 181) for the VF area, and between 0.6 and 6.0 ms (3.64 +/- 1.14, N = 144) for the FM-FM area. More neurons in the VF area than those in the FM-FM area showed no response or a poor response to the TPS stimulus. Therefore VF neurons are less suited than neurons in the FM-FM area for processing target ranges in the terminal phase of target-directed flight. Facilitative delay-tuning curves were commonly sandwiched between inhibitory delay-tuning curves. The lack of response or poor response to the TPS stimulus can be explained by this inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Projections from the primary auditory cortex onto the dorsal cortex of the inferior colliculus in albino rats.

The topography of connections from the primary auditory cortex (Te1) onto the dorsal cortex (DC) of the inferior colliculus (IC) was studied using the anterograde neural tracers Phaseolus vulgaris (PHA-L) and Biotinylated dextran amine (BDA). Injections in different restricted portions of the ventral Te1 showed labelled axonal sheets in the ipsilateral DC with extensions in the central nucleus and the external cortex. Also contralateral labelled axons were found with a patchy appearance. The pattern of labelled axonal laminae is arranged in an orderly fashion, so that a correlation exists between the injection field (antero-to caudoventral injections) and the pattern of labelled axonal sheets (from a ventromedial to a dorsolateral arrangement) in the IC. However, variations from this pattern were observed. Also only the injections made in rostral and middle parts of Te1 V are orderly arranged in the territory of the DC, while the Te1 V caudoventral projection partially overlaps those from antero and mid-central regions. A topographical arrangement in the fibre projection from the medial and dorsal zones of Te1 (Te1 D) exists in the neuropil of the IC. The bands from Te1 D overlapped with the bands from Te1 V but in different order. This indicates that the projection of the mid-dorsal zone of Te1 is not topographically arranged in the DC like Te1 V. Based on the results we have obtained, there is strong evidence that the projection from Te1 V to the DC is topographically organized in a rostrocaudal sequence which gives definite terminal fields. However, each of these fields (medial, central and external) receives a principal bulk of primary auditory cortical fibres and a supplementary one. This implies that territories of the DC which contain neurons responsive to low frequencies receive a projection from Te1 fields with neurons which are responsive to high or to low frequencies.

Acoustic Stimulation↗

Anatomical and functional imaging of the auditory cortex in awake mustached bats using magnetic resonance technology.

The auditory cortex of mustached bats, Pteronotus parnellii, has been studied extensively using neuroanatomical tract-tracing and electrophysiological techniques to elucidate the functional organization and neural mechanisms important for auditory processing. While these techniques have identified several cortical maps involved in processing auditory information, there has been no direct observation of the dynamics of simultaneous activation of several discrete areas. We applied magnetic resonance (MR) imaging techniques for visualizing brain structures in awake bats using a 7-Tesla magnet system; we also investigated functional MR imaging by measuring changes in stimulus-correlated blood oxygenation levels to detect cortical areas exhibiting evoked neural activity. High resolution (100 microm) anatomical images were successfully acquired without any motion artifacts. It was possible to reconstruct the whole brain image and analyze brain surface structures with three dimensional (3D) MR imaging data. These data provide detailed morphometric measurements that will allow localization of stimulus specific neural activity patterns using modified functional magnetic-resonance-imaging (fMRI) protocols. Motion artifacts is the primary disadvantage of using awake bats; our study shows that fMRI of a bat's brain is feasible and may prove to be an important advancement for a further understanding of auditory processing in this species.Themes: Sensory systems, Neural basis of behavior.

Acoustic Stimulation↗

Effects of quinine on neural activity in cat primary auditory cortex.

The effect of systemically applied quinine on single-unit firing activity in primary auditory cortex was investigated in seven cats. A dose of 100 or 200 mg/kg of quinine hydrochloride was administered intramuscularly and recordings from the same units were performed prior to application and continuously up to on average 5.5 h after administration. All animals showed 10-40 dB of threshold shift about 30 min after administration and some animals showed recovery during the course of the investigation. Significant increases were found in spontaneous firing rates for low-firing-rate units (initial firing rate < 1 spike/s). For high-firing-rate units (initial firing rate > 1 spike/s) no significant changes were observed. There were no significant changes in modal and mean interspike interval. The time-to-rebound peak in the autocorrelation function for spontaneous firings was not altered significantly. The rate of burst occurrence showed no significant change. The best modulation frequency in response to stimulation with periodic click trains decreased after administration, but the limiting rate did not change. Peak cross-correlation coefficients for the spontaneous firings of simultaneously recorded cells showed a significant increase and the correlogram's central peak was significantly narrower after quinine application. Dose effects were only present for cross-correlation results and temporal modulation transfer functions. The results for both spontaneous firing rate, peak width in the cross-correlogram and click stimulation were similar to those observed in salicylate-treated cats (Ochi and Eggermont, 1996). The other findings were different from those observed after salicylate. It is obvious that the effects of quinine on the auditory system are not the same as those of salicylate. The increased synchronization of the spontaneous firings across different neurons observed after application of both drugs may be related to tinnitus.

Acoustic Stimulation↗

Active listening: task-dependent plasticity of spectrotemporal receptive fields in primary auditory cortex.

Listening is an active process in which attentive focus on salient acoustic features in auditory tasks can influence receptive field properties of cortical neurons. Recent studies showing rapid task-related changes in neuronal spectrotemporal receptive fields (STRFs) in primary auditory cortex of the behaving ferret are reviewed in the context of current research on cortical plasticity. Ferrets were trained on spectral tasks, including tone detection and two-tone discrimination, and on temporal tasks, including gap detection and click-rate discrimination. STRF changes could be measured on-line during task performance and occurred within minutes of task onset. During spectral tasks, there were specific spectral changes (enhanced response to tonal target frequency in tone detection and discrimination, suppressed response to tonal reference frequency in tone discrimination). However, only in the temporal tasks, the STRF was changed along the temporal dimension by sharpening temporal dynamics. In ferrets trained on multiple tasks, distinctive and task-specific STRF changes could be observed in the same cortical neurons in successive behavioral sessions. These results suggest that rapid task-related plasticity is an ongoing process that occurs at a network and single unit level as the animal switches between different tasks and dynamically adapts cortical STRFs in response to changing acoustic demands.

Animals↗

Sound sequence discrimination learning motivated by reward requires dopaminergic D2 receptor activation in the rat auditory cortex.

We have previously reported that sound sequence discrimination learning requires cholinergic inputs to the auditory cortex (AC) in rats. In that study, reward was used for motivating discrimination behavior in rats. Therefore, dopaminergic inputs mediating reward signals may have an important role in the learning. We tested the possibility in the present study. Rats were trained to discriminate sequences of two sound components, and licking behavior in response to one of the two sequences was rewarded with water. To identify the dopaminergic inputs responsible for the learning, dopaminergic afferents to the AC were lesioned with local injection of 6-hydroxydopamine (6-OHDA). The injection attenuated sound sequence discrimination learning, while it had no effect on discrimination between the sound components of the sequence stimuli. Local injection of 6-OHDA into the nucleus accumbens attenuated sound discrimination learning. However, not only discrimination learning of sound sequence but also that of the sound components were impaired. SCH23390 (0.2 mg/kg, i.p.), a D1 receptor antagonist, had no effect on sound sequence discrimination learning, while it attenuated the licking behavior to unfamiliar stimuli. Haloperidol (0.5 mg/kg, i.p.), a D2 family antagonist, attenuated sound sequence discrimination learning, while it had no clear suppressive effect on discrimination of two different sound components and licking. These results suggest that D2 family receptors activated by dopaminergic inputs to the AC are required for sound sequence discrimination learning.

Acoustic Stimulation↗