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Differential effects of acetylcholine on neuronal activity and interactions in the auditory cortex of the guinea-pig.

During normal brain operations, cortical neurons are subjected to continuous cholinergic modulations. In vitro studies have indicated that, in addition to affecting general cellular excitability, acetylcholine also modulates synaptic transmission. Whether these cholinergic mechanisms lead to a modulation of functional connectivity in vivo is not yet known. Herein, the effects were studied of an iontophoretic application of acetylcholine and of the muscarinic agonist, carbachol, on the ongoing activity and co-activity of neurons simultaneously recorded in the auditory cortex of the anaesthetized guinea-pig. Iontophoresis of cholinergic agonists mainly affected the spontaneous firing rates of auditory neurons, affected autocorrelations less (in most cases their central peak areas were reduced), and rarely affected cross-correlations. These findings are consistent with cholinergic agonists primarily affecting the excitability of cortical neurons rather than the strength of cortical connections. However, when changes of cross-correlations occurred, they were usually not correlated with concomitant changes in average firing rates nor with changes in autocorrelations, which suggests a secondary cholinergic effect on specific cortico-cortical or thalamo-cortical connections.

Acetylcholine↗

Target range-sensitive neurons in the auditory cortex of the mustache bat.

Echolocating bats determine distance to targets by the time delay between their emitted biosonar pulses and the returning echoes. By varying the delay between synthetic pulses and echoes in stimulus pairs at various repetition rates and durations, neurons have been found in the auditory cortex of the mustache bat (Pteronotus parnellii rubiginosus) which are sensitive to target range during the search, approach, and terminal phases of prey capture or landing. Two classes of range-sensitive neurons were found: (i) tracking neurons, whose best delay for response to an echo following the emitted pulse becomes shorter and narrower as the bat closes in on the target, and (ii) range-tuned neurons, whose best delay is constant, and which respond to the target only when it is within a certain narrow fixed range. Range-tuned neurons are specialized for processing echoes only during a particular period of the search, approach, or terminal phases of echolocation, and they provide support for a theory of ranging in bats that incorporates groups of neurons with a spectrum of preferred echo delays to detect target distance.

Action Potentials↗

Measurements of the temporal fMRI response of the human auditory cortex to trains of tones.

Averaged single trials (AST) allowed the functional magnetic resonance imaging (fMRI) response to auditory stimuli to be measured at high temporal (1 s) and spatial (0.1 cm3) resolution. Using this paradigm we investigated the transient signal response to 100-ms tone bursts in trains of between 100 ms and 25.5 s in total duration. We have demonstrated that the fMRI response to such auditory stimuli is approximately linear for trains of 6 s and longer, but that shorter stimuli produce signals that are larger than might be expected from the response to the longer stimuli. This nonlinear behavior can be modeled if an adaptive response to each stimulus is assumed. A study using a novel paradigm was also performed in order to study the influence of scanner noise during fMRI experiments on the auditory system response to tones. This study demonstrated that the temporal response to 700-ms tone stimuli is modified when performed in the presence of scanner gradient noise, the modification being a small but significant increase (P < 0.05) in the magnitude of the response. Finally the ability to measure the onset of functional activation using the AST method was examined. It was found, with the aid of computer simulation that a sampling rate of one image per second is adequate to distinguish temporal responses. Using the data acquired in this study, onset times were calculated for the auditory cortex, and these results are consistent with current models of functional activation.

Adult↗

Reward-dependent plasticity in the primary auditory cortex of adult monkeys trained to discriminate temporally modulated signals.

Adult owl monkeys were trained to detect an increase in the envelope frequency of a sinusoidally modulated 1-kHz tone. Detection was positively correlated with the magnitude of the change in the envelope frequency. Surprisingly, neuronal responses recorded in the primary auditory cortex of trained monkeys were globally suppressed by the modulated tone. However, the contrast in neuronal responsiveness to small increases versus large increases in envelope frequencies was actually enhanced in the trained animals. The results suggest behaviorally contingent inhibitory and excitatory processes that are modulated by the probability that a particular signal predicts a reward.

Animals↗

The effect of pulse repetition rate on the delay sensitivity of neurons in the auditory cortex of the FM bat, Myotis lucifugus.

1. Echo delay is the primary cue used by echolocating bats to determine target range. During target-directed flight, the repetition rate of pulse emission increases systematically as range decreases. Thus, we examined the delay tuning of 120 neurons in the auditory cortex of the bat, Myotis lucifugus, as repetition rate was varied. 2. Delay sensitivity was exhibited in 77% of the neurons over different ranges of pulse repetition rates (PRRs). Delay tuning typically narrowed and eventually disappeared at higher PRRs. 3. Two major types of delay-sensitive neurons were found: i) delay-tuned neurons (59%) had a single fixed best delay, while ii) tracking neurons (22%) changed their best delay with PRR. 4. PRRs from 1-100/s were represented by the population of delay-sensitive neurons, with the majority of neurons delay-sensitive at PRRs of at least 10-20/s. Thus, delay-dependent neurons in Myotis are most active during the search phase of echolocation. 5. Delay-sensitive neurons that also responded to single sounds were common. At PRRs where delay sensitivity was found, the responses to single sounds were reduced and the responses to pulse-echo pairs at particular delays were greater than the single-sound responses. In facilitated neurons (53%), the maximal delay-dependent response was always larger than the best single-sound responses, whereas in enhanced neurons (47%), these responses were comparable. The presence of neurons that respond maximally to single sounds at one PRR and to pulse-echo pairs with particular echo delays at other PRRs suggests that these neurons perform echo-ranging in conjunction with other biosonar functions during target pursuit.

Acoustic Stimulation↗

Event-related dimensional reductions in the primary auditory cortex of the conscious cat are revealed by new techniques for enhancing the non-linear dimensional algorithms.

The analytic algorithms derived from non-linear deterministic models may be more sensitive to differences in physiological data than those based on linear stochastic models. Among the non-linear algorithms the time-dependent dimensional ones appear to be the most sensitive discriminators. In the present study dimensional responses were examined in both electronically and mathematically generated data and in high-resolution physiological data. The latter were event-related potentials (ERPs) recorded from the primary auditory cortex of cats during classical conditioning. Two techniques were found to lengthen and stabilize the linear scaling region in the correlation integral of the dimensional algorithms: (1) linking trials to increase data length; and (2) gain reduction to lower integer-values of noise, combined with algorithmic setting of slopes < 0.5 to zero. Of the three dimensional algorithms examined, only the time-dependent Point Correlation Dimension (PD2i) showed low error rates when tracking the dimensional shifts in non-stationary generated data. This algorithm also uniquely distinguished between the conditioned and unconditioned physiological responses. The ERPs had corresponding PD2i's that were significantly different from each other as well as from their own randomized-phase surrogates. The brief dimensional reduction that follows a conditioned stimulus is interpreted to be related to 'cooperativity' among the underlying cortical neurons that contribute to its electrogenesis.

Algorithms↗

Neural correlates of instrumental learning in primary auditory cortex.

In instrumental learning, Thorndike's law of effect states that stimulus-response relations are strengthened if they occur prior to positive reinforcement and weakened if they occur prior to negative reinforcement. In this study, we demonstrate that neural correlates of Thorndike's law may be observed in the primary auditory cortex, A1. Adult owl monkeys learned to discriminate tones higher than a standard frequency. Responses recorded from implanted microelectrodes initially exhibited broad spectral selectivity over a four-to-five octave range. With training, frequency discrimination thresholds changed from close to one octave to about 1/12 octave. Physiological recordings during the week in which the monkey came under behavioral control signaled by a drop in measured threshold had stronger responses to all frequencies. During the same week, A1 neural responses to target stimuli increased relative to standard and nontarget stimuli. This emergent difference in responsiveness persisted throughout the subsequent weeks of behavioral training. These data suggest that behavioral responses to stimuli modulate responsiveness in primary cortical areas.

Animals↗

High-resolution multiple-unit EEG in cat auditory cortex reveals large spatio-temporal stochastic interactions.

It has been argued that information processing in the cortex is optimised with regard to certain information theoretic principles. We have, for instance, recently shown that spike-timing dependent plasticity can improve an information-theoretic measure called spatio-temporal stochastic interaction which captures how strongly a set of neurons cooperates in space and time. Systems with high stochastic interaction reveal Poisson spike trains but nonetheless occupy only a strongly reduced area in their global phase space, they reveal repetiting but complex global activation patterns, and they can be interpreted as computational systems operating on selected sets of collective patterns or "global states" in a rule-like manner. In the present work we investigate stochastic interaction in high-resolution EEG-data from cat auditory cortex. Using Kohonen maps to reduce the high-dimensional dynamics of the system, we are able to detect repetiting system states and estimate the stochastic interaction in the data, which turns out to be fairly high. This suggests an organised cooperation in the underlying neural networks which cause the data and may reflect generic intrinsic computational capabilities of the cortex.

Animals↗

Reorganization in the auditory cortex of the rat induced by intracortical microstimulation: a multiple single-unit study.

Many manipulations are able to change or perturb various aspects of single neuron properties and interneuronal relationships. Changes of cerebral cortex organization have been observed in different cortical areas and at different time scales in relation to peripheral stimulation, peripheral damage, associative learning, and electrical stimulation. Here we describe studies on separable multineuron recordings in the rat's auditory cortex under two different anesthetics. Acoustic stimuli were used as a normal, physiological input, and weak electrical intracortical microstimulation (ICMS) as a perturbation that forces a rapid cortical reorganization. ICMS induced fast changes in the cortical map and in the receptive field properties of cells at the electrically stimulated and adjacent electrodes. In effect there was an enlargement of the cortical domain tuned to the acoustic frequency that had been represented at the stimulating electrode. ICMS also incremented afterdischarge responses; these consisted of an initial response to the auditory stimulus followed by less intense repetitive activity that was stimulus-time locked and had a period of 8-12 Hz, similar to that of the spontaneous synchronous activity. Cortical activity under ketamine differed from that under pentobarbital sodium, although in both situations we observed that cortical neurons were highly synchronous.

Acoustic Stimulation↗

Listening through different ears alters spatial response fields in ferret primary auditory cortex.

The localization of sounds in space is based on spatial cues that arise from the acoustical properties of the head and external ears. Individual differences in localization cue values result from variability in the shape and dimensions of these structures. We have mapped spatial response fields of high-frequency neurons in ferret primary auditory cortex using virtual sound sources based either on the animal's own ears or on the ears of other subjects. For 73% of units, the response fields measured using the animals' own ears differed significantly in shape and/or position from those obtained using spatial cues from another ferret. The observed changes correlated with individual differences in the acoustics. These data are consistent with previous reports showing that humans localize less accurately when listening to virtual sounds from other individuals. Together these findings support the notion that neural mechanisms underlying auditory space perception are calibrated by experience to the properties of the individual.

Acoustic Stimulation↗

Linking sight and sound: fMRI evidence of primary auditory cortex activation during visual word recognition.

We describe two studies that used repetition priming paradigms to investigate brain activity during the reading of single words. Functional magnetic resonance images were collected during a visual lexical decision task in which nonword stimuli were manipulated with regard to phonological properties and compared to genuine English words. We observed a region in left-hemisphere primary auditory cortex linked to a repetition priming effect. The priming effect activity was observed only for stimuli that sound like known words; moreover, this region was sensitive to strategic task differences. Thus, a brain region involved in the most basic aspects of auditory processing appears to be engaged in reading even when there is no environmental oral or auditory component.

Adolescent↗

Activation of association auditory cortex demonstrated with functional MRI.

Activations in the temporal lobes previously observed using positron emission tomography and auditory stimuli were partially reproduced with functional MRI and echo-planar imaging at 1.5 T in six volunteers performing tone and phoneme monitoring tasks. Verbal processing compared to a tone recognition task significantly activated a cortical area located in the left anterior temporal region (P < 0.02).

Adult↗

Echo-location of bats after ablation of auditory cortex.

1. Echo-location of blinded Yuma bats (Myotis yumanensis) was studied after ablation of the auditory cortex (A.C.). A task of obstacle-avoidance was given to the bats. Hits and misses of strands were counted, and orientation sounds emitted by the bats during flight were recorded.2. After bilateral ablation of A.C., two bats out of six failed to avoid even large obstacles such as 3.7 mm strands and wall. These bats emitted orientation sounds at a rate of 10-15/sec during flight, but did not change that rate before crossing the obstacles and crashed into them. In these bats, other cortical areas in addition to A.C. were probably ablated.3. In three bats out of six, obstacle-avoidance performance was quite normal. These bats avoided even 0.2 mm strands with orientation sounds, the repetition rate of which was systematically increased before crossing the obstacles. In two of them, the dorsal half of the inferior colliculus (I.C.) was bilaterally ablated in addition to A.C. But ability to avoid the obstacles was not impaired at all. Their cerebral cortices did not show the normal positive-negative diphasic potential change in response to tonal stimuli, although the normal diphasic potential change was retained in A.C. of bats which could not echo-locate as a result of bilateral ablation of the main nucleus of I.C. A.C. appeared to be not essential for echo-location.4. Unilateral ablation of A.C. and the internal capsule had no effect on echo-location, but bilateral ablation of them usually resulted in death from operational trauma.5. It was suggested that A.C. was less important for sound localization in bats than in cats.

Journal Article↗

Recruitment of the auditory cortex in congenitally deaf cats by long-term cochlear electrostimulation.

In congenitally deaf cats, the central auditory system is deprived of acoustic input because of degeneration of the organ of Corti before the onset of hearing. Primary auditory afferents survive and can be stimulated electrically. By means of an intracochlear implant and an accompanying sound processor, congenitally deaf kittens were exposed to sounds and conditioned to respond to tones. After months of exposure to meaningful stimuli, the cortical activity in chronically implanted cats produced field potentials of higher amplitudes, expanded in area, developed long latency responses indicative of intracortical information processing, and showed more synaptic efficacy than in naïve, unstimulated deaf cats. The activity established by auditory experience resembles activity in hearing animals.

Acoustic Stimulation↗

Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex.

Cortical sensitivity in representations of behaviorally relevant complex input signals was examined in recordings from primary auditory cortical neurons (AI) in adult, barbiturate-anesthetized common marmoset monkeys (Callithrix jacchus). We studied the robustness of distributed responses to natural and degraded forms of twitter calls, social contact vocalizations comprising several quasi-periodic phrases of frequency and AM. We recorded neuronal responses to a monkey's own twitter call (MOC), degraded forms of their twitter call, and sinusoidal amplitude modulated (SAM) tones with modulation rates similar to those of twitter calls. In spectral envelope degradation, calls with narrowband channels of varying bandwidths had the same temporal envelope as a natural call. However, the carrier phase was randomized within each narrowband channel. In temporal envelope degradation, the temporal envelope within narrowband channels was filtered while the carrier frequencies and phases remained unchanged. In a third form of degradation, noise was added to the natural calls. Spatiotemporal discharge patterns in AI both within and across frequency bands encoded spectrotemporal acoustic features in the call although the encoded response is an abstract version of the call. The average temporal response pattern in AI, however, was significantly correlated with the average temporal envelope for each phrase of a call. Response entrainment to MOC was significantly correlated with entrainment to SAM stimuli at comparable modulation frequencies. Sensitivity of the response patterns to MOC was substantially greater for temporal envelope than for spectral envelope degradations. The distributed responses in AI were robust to additive continuous noise at signal-to-noise ratios > or =10 dB. Neurophysiological data reflecting response sensitivity in AI to these forms of degradation closely parallel human psychophysical results on the intelligibility of degraded speech in quiet and noisy conditions.

Acoustic Stimulation↗

Changes in auditory cortex parallel rapid perceptual learning.

Learning perceptual skills is characterized by rapid improvements in performance within the first hour of training (fast perceptual learning) followed by more gradual improvements that take place over several daily practice sessions (slow perceptual learning). Although it is widely accepted that slow perceptual learning is accompanied by enhanced stimulus representation in sensory cortices, there is considerable controversy about the neural substrates underlying early and rapid improvements in learning perceptual skills. Here we measured event-related brain potentials while listeners were presented with 2 phonetically different vowels. Listeners' ability to identify both vowels improved gradually during the first hour of testing and was paralleled by enhancements in an early evoked response ( approximately 130 ms) localized in the right auditory cortex and a late evoked response ( approximately 340 ms) localized in the right anterior superior temporal gyrus and/or inferior prefrontal cortex. These neuroplastic changes depended on listeners' attention and were preserved only if practice was continued; familiarity with the task structure (procedural learning) was not sufficient. We propose that the early increases in cortical responsiveness reflect goal-directed changes in the tuning properties of auditory neurons involved in parsing concurrent speech signals. Importantly, the neuroplastic changes occurred rapidly, demonstrating the flexibility of human speech segregation mechanisms.

Acoustic Stimulation↗