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Basal forebrain stimulation modifies auditory cortex responsiveness by an action at muscarinic receptors.

We have hypothesized that auditory cortex plasticity involves modification of thalamocortical transmission by basal forebrain (BF) cholinergic neurons, and that this action may involve muscarinic receptors. In a first test of this hypothesis, we report that BF stimulation can suppress or facilitate, depending on the intensity of stimulation, auditory cortical responses elicited by thalamic stimulation. BF-mediated facilitation is antagonized by atropine, implicating muscarinic receptors. These data suggest that BF cholinergic neurons functionally modify auditory cortex by regulating thalamocortical transmission.

Animals

Effects of unilateral ablation of auditory cortex on monaural cat's ability to localize sound.

1. Cats with one cochlea destroyed were trained to localize sound. After behavioral measures of the animal's accuracy of localization were made, cortical auditory areas were ablated unilaterally. 2. The results showed: a) like binaural localization, monaural localization of sound in space, as measured by the ability of an animal to move toward a sound source, depends on integrity of auditory cortex; b) it is only ablation of cortex contralateral to the functional ear that seriously affects localizing behavior; ablation of cortex ipsilateral to the intact cochlea has little or no effect on localizing behavior. 3. To explain the results, we suggest that auditory cortex is essential for an organized perception of space including the relation of the animal's position to other objects in space. We also suggest that auditory cortex contralateral to a given ear is necessary in order for the animal to recognize that a stimulus is presented to that ear of, when both ears are intact, to recognize that the stimulus to the given ear differs in some way (intensity, time of arrival, sequential arrangement of sounds) from the stimulus to the opposite ear.

Animals

Effect of unilateral and bilateral auditory cortex lesions on the discrimination of vocalizations by Japanese macaques.

Ten Japanese macaques were trained to discriminate between two types of Japanese macaque coo vocalizations before and after auditory cortex ablation. Five of the animals were tested following left unilateral ablation, whereas the other five were tested following right unilateral ablation. After postoperative testing, symmetrical lesions were made in the remaining hemisphere in two animals from each group and the effect of bilateral lesions was assessed. The animals were tested using a shock avoidance procedure. Unilateral ablation of left auditory cortex consistently resulted in an initial impairment in the ability to discriminate between the vocalizations with the animals regaining normal performance in 5-15 sessions. In contrast, right unilateral ablation had no detectable effect on the discrimination. Bilateral auditory cortex ablation rendered the animals permanently unable to discriminate between the coos. Although the monkeys could learn to discriminate the coos from noise and from 2- and 4-kHz tones, they had great difficulty in discriminating between the coos and tones in the same frequency range as the coos (i.e., 500 Hz and 1 kHz). The initial impairment following left unilateral lesions indicates that the ability to perceive species-specific vocalizations is lateralized to the left hemisphere. The observation that bilateral lesions abolish the discrimination indicates that the recovery in the left lesion cases was the result of the right hemisphere mediating the discrimination.

Animals

The laminar organization of the prospective auditory cortex in the human fetus (11--13.5 weeks of gestation).

The prospective auditory cortex was analysed in human fetuses at 11--13,5 post-ovulatory weeks with Nissl, Golgi and E.M. techniques. At 11--12 weeks, marginal, cortical plate, intermediate, subventricular and ventricular layers were recognized. Post-migratory neurons with developing dendrites were seen in marginal layer, cortical plate and superficial part of the intermediate zone only. At 12--13,5 weeks the superficial part of the intermediate zone is transformed into the true cortical layer--"subplate layer"--characterized by maturing neurons with growing dendrites, fine axonal arborization and low cell density. The neuronal circuitry elements are thus present very early in the prospective auditory cortex and distributed throughout the deep cortical plate of the "subplate layer" corresponding to the synaptic territory of other areas of the human fetal cortex.

Auditory Cortex

Magnetic responses of the human auditory cortex to noise/square wave transitions.

We recorded evoked magnetic fields from the human auditory cortex to noise/square wave sequences. Two prominent deflections were observed: one 100 msec after the noise onset (N100m) and another 100 msec after the noise/square wave transition (N100m'). The amplitude of N100m' increased with decrease in square wave frequency from 2 kHz to 0.125 kHz and with increase in square wave duration from 4 msec to 200 msec. The latency of N100m' was on the average 23 msec longer for noise durations of 60 msec than 310 msec, whereas the amplitude of N100m' did not change. Increase in interstimulus interval from 1.1 to 8.8 sec enhanced the amplitude of N100m significantly more than that of N100m'. The small interaction between N100m and N100m' and their different recovery cycles suggest that different activation patterns underlie these two 100 msec responses at the auditory cortex.

Adult

[A histochemical study of acetylcholinesterase in intact and deafferented cat auditory cortex].

The peculiarities of the AChE distribution were investigated in the intact cat auditory cortex and during early period of its neuronal isolation. It is shown that in the isolated cortex slab the staining of the AChE containing fibre disappeared from the neuropile, while in the intact cortex it was well pronounced. AChE accumulation was observed in the proximal parts of the transsected thalamo-cortical fibres. It is supposed that the AChE-containing fibres in the auditory cortex belong to nonspecific thalamic inputs.

Acetylcholinesterase

Reactions of human auditory cortex to a change in tone duration.

Auditory evoked magnetic fields were measured using a stimulation sequence where repetitive identical tone bursts were randomly and infrequently replaced by shorter tones. The deviation in the stimulus duration evoked a specific response, the mismatch field, peaking about 130 ms after the end of the shorter stimulus. The response can be explained by neural activity at the supratemporal auditory cortex. The results suggest the existence of a neural mechanism specific to changes in sound duration.

Acoustic Stimulation

[Comparative study of interneuronal relations in the auditory cortex of awake and anesthetized cats].

The character of interneuronal relations in the auditory cortex of alert and anaesthetized cats (nembutal) with chronicly inplanted electrodes was studied with the method of statistic analysis of cross-intervals of the two impulse series. The analysis of the histograms, obtained by means of processing a neuronal activity, showed that nembutal did not eliminate the dependent relations between neurones and that in the majority of cases the types of these relations are either retained or supplemented with new components. Experiments with a reduced dose of nembutal permitted to trace in time the changes in the amount of the inhibitory and excitatory interrelations in the anaesthetized state, and to compare these changes to the changes in the frequency of spike activity. It was found that nembutal predominantly suppresses the activity of the neurones, generating small spikes. The number of inhibitory connections is reduced simultaneously. Such synchroneity permits to assume the participation of the neurones generating small spikes in the establishment of inhibitory interrelations in the cat auditory cortex.

Anesthesia, General

Ferrier and the study of auditory cortex.

David Ferrier was a British physician who studied the localization of function in the cerebral hemispheres during the latter half of the 19th century. Using stimulation and ablation techniques, Ferrier demonstrated that auditory cortex was located in the superior temporal gyrus of the monkey and that ablation of auditory cortex resulted in deafness. Although he was substantially correct, Ferrier's location of auditory cortex was not accepted by his contemporaries, and his observations of cortical deafness were, until recently, discounted by modern researchers. Just why his findings were rejected is of interest to the study of cortical function.

Auditory Cortex

Role of context in the expression of learning-induced plasticity of single neurons in auditory cortex.

Classical conditioning produces frequency-specific plasticity of receptive fields (RFs) of single neurons in cat auditory cortex (Diamond & Weinberger, 1986). In this article we show that although plasticity may be observed during both training trials and determination of RFs, it is usually expressed in a qualitatively different form (e.g., decreased response during conditioning vs. increased response to this same conditioned stimulus in the postconditioning RF). This differential expression of learning-induced plasticity provides evidence for a role of context in neurophysiological mechanisms of learning in auditory cortex. A model of cortical neurons functioning within a mosaic of influences is presented. The Functional Mosaic model views the induction and expression of plasticity as separate processes.

Animals

Extrathalamic ascending projections to physiologically identified fields of the cat auditory cortex.

The neurons of origin of ascending extrathalamic projections to the auditory cortex were labeled retrogradely with WGA-HRP injected in physiologically identified auditory cortical fields of the cat (anterior (AAF), primary (AI), posterior (PAF) and secondary (AII) fields). After injection in the tonotopically organized auditory cortical fields (AAF, AI and PAF), labeled neurons were distributed in 7 extrathalamic subcortical regions included in one or the other of 2 distinct systems of ascending projections to the neocortex. In the 'diffuse' system of projection, labeled neurons were observed bilaterally in the locus coeruleus, the nuclei of the raphe, the lateral hypothalamus, ipsilaterally in the ventromedial mesencephalic tegmentum and the basal forebrain; in the 'accessory sensory' system of projection, labeled neurons were found ipsilaterally in the nucleus of the brachium of the inferior colliculus and bilaterally in the claustrum. After injection in AII, labeled neurons were seen only in the 'diffuse' system of projection. For AAF and AI, the major contribution to the total extrathalamic ascending input originated from the lateral hypothalamus, whereas for AII it was the locus coeruleus. In contrast, PAF received extrathalamic ascending inputs mainly from the claustrum. Anterogradely labeled corticofugal terminal fields were found only in the nucleus of the brachium of the inferior colliculus and, after injection in PAF, in the claustrum.

Acetylcholine

Foetal and neonatal development of evoked responses in guinea-pig auditory cortex.

Development of the response of the auditory cortex to unilateral acoustic stimulation by a chick was studied in guinea-pig foetuses from the 50th day to the end of gestation and in newborn animals. The first cortical response appeared on the 52nd to 53rd day of gestation. The maximum responses were concentrated in the temporal cortex, between the somatosensory (parietal) and optic (occipital) area. The progressive development of the latent period of the cortical response and of its various components distinctly slowed down on the last days of gestation. At the same time, the amplitude of the cortical response was temporarily augmented. The cortical response developed from a simple negative wave in the youngest embryos into an intricate complex with an initial positive component in newborn guinea-pigs. The basic components of this complex were already discernible on the 64th to 65th day of gestation. The ability to react to repeated peripheral stimulation of 0.1-2 c/s frequency increased with foetal age, with temporary deterioration on the last days of gestation. Resistance of the cortical auditory response to cerebral anoxia rose up to term, with a temporary drop from the 64th day of gestation. After the initiation of independent respiration, cerebral hypoxia and bilateral vagotomy chiefly influenced the stability of the more recent components of the cortical auditory response in mature foetuses.

Acoustic Stimulation

Modification of neuromagnetic responses of the human auditory cortex by masking sounds.

We have studied the effects of masking sounds on auditory evoked magnetic fields (AEFs) of healthy humans. The AEFs were elicited by 25-ms tones presented randomly to the left or to the right ear, and the responses were recorded over the right auditory cortex. Without masking, the 100-ms deflection (N100m) was of somewhat higher amplitude and of shorter latency for contra- than ipsilateral stimuli. Continuous speech, music, or intermittent noise, delivered to the left ear, dampened N100m to stimulation of both ears without correlated changes in sensation. Intermittent noise had a weaker effect on N100m than speech or music. Continuous noise fed to the left ear dampened both the sensation of and the responses to the left-ear stimuli, with no significant effect on the responses to the right-ear stimuli. The results suggest that the masking effects of continuous noise, seen at the auditory cortex, derive mainly from the periphery whereas the effects of sounds with intensity and frequency modulations take place at more central auditory pathways.

Acoustic Stimulation

Age-related deterioration of pyramidal cell basal dendrites in rat auditory cortex.

The basal dendritic trees of layer V pyramidal cells in the rat auditory cortex were examined quantitatively in a group of 3-month-old and a group of 34- and 36-month-old rats. Two forms of analysis were used on the Golgi preparations: (1) the number of intersections between the basal dendrites and a series of concentric circles whose common center lies over the perikaryon center, and (2) the number of dendritic branches, by order, per neuron. The data indicate that in the old animals the density of the dendritic tree has decreased significantly within a radius of about 150mu of the perikaryon, yet the extent of the dendritic domain has not changed appreciably. Analysis of the dendritic branching suggests that there has been a deterioration not only in the peripheral branches of the dendritic tree, but also that entire dendrites have been lost. This loss of primary branches was confirmed through the reconstruction of layer V neuronal perikarya and their proximal dendrites from 1-mu plastic serial sections of auditory cortex. Concomitant with the loss of dendrites which accompanies advancing age is a tendency for the perikaryon to be smaller, but not distorted, in the old animals.

Aging

A study on the tonotopic organization in the auditory cortex of the cat; an application of the glycine labelling method.

3H-glycine was locally applied to the auditory cortex of chloralose anaesthetized cats. Upon tonal stimulation the 3H-glycine was taken up and incorporated into the proteins of nerve cells. The selectively activated neurons were visualized by serial light microscopic autoradiography. Systematic application of this experimental setup revealed tonotopic organization in the primary auditory cortex. The distribution of nerve cells responding to spectrally pure, continuous tones of 0.34, 3.3, 8.0, 16 and 30 kHz was mapped. At these frequencies, distinct but overlapping representations were found, whose area increased in parallel with the elevation of frequencies. Tone pips and ramp stimuli resulted in generalized labelling, independently of pitch.

Animals

[The connections of the parietal cortex with the lateral suprasylvian gyrus (the Clare-Bishop field) and the auditory cortex in the cat].

It has been shown that a parietal projection to the Clare--Bishop area is moderate and organized in a topographic manner. Associative fibres of area 5 terminate in the anterior part of the Clare--Bishop area, which corresponds to the intermediate and anterior part of the posterior suprasylvian sulcus belt. Area 7 projects to the posterior part of the intermediate and posterior suprasylvian sulcus belt. Area 5 and 7 send a few fibres to the auditory cortex. Associative fibres of area 5 terminate in the middle ectosylvian and sylvian gyri: areas 22, 50. Area 7 is connected only with the superior extremity of the middle ectosylvian gyrus or of areas 22, 50.

Afferent Pathways

Auditory cortex of the long-eared hedgehog (Hemiechinus auritus): II. Tuning properties.

The forebrain of hedgehogs is considered by many investigators as one of the simplest and most primitive among extant placental mammals. In a recent study we have shown that the auditory cortex of the long-eared hedgehog (Hemiechinus auritus) comprises two distinct auditory fields, which are tonotopically organized. In this study, we describe tuning properties of single cells in these two fields. Application of the Q10dB and Square Root measures for determining sharpness of tuning revealed that, although most of the cells in the more anterior field, which is considered primary, are sharply tuned, on the average they are more broadly tuned than cells in the primary auditory cortex of other mammals. In the posterior field, the distribution of narrowly and broadly tuned cells is equal. Narrowly tuned cells in both fields are equally narrow, as are the broadly tuned cells. Latencies of single cells in both fields are frequency and intensity dependent and are somewhat longer than these found in other mammals. The distribution of BFs vs. threshold intensity matches fairly well the behavioral audiogram previously described. Our findings suggest that, in spite of the view that the isocortex of hedgehogs represents a 'primitive' condition, some basic tuning properties of their auditory cortex cells are comparable to those of other mammals.

Animals

Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques.

1. The ability of four Japanese macaques (Macaca fuscata) to localize sound was determined after bilateral ablation of auditory cortex. The animals were given two tests: a "midline" test in which they had to discriminate noise bursts presented from a loudspeaker located to the left from identical noise bursts presented from a loudspeaker located to the right of midline, and a "hemifield" test in which both loudspeakers were located in their right hemifield. 2. Both of the tests were administered by the use of two different behavioral tasks: a conditioned-avoidance task in which the animals were trained to make or break contact with a water spout to indicate the location of a sound source, and a two-choice task that required the animals to walk to the source of the sound. 3. The results of both the conditioned-avoidance and the two-choice tasks demonstrated that the animals were able to perform the midline discrimination although their localization acuity was reduced. However, the animals had great difficulty in learning to walk to the source of a sound in spite of the fact that they had received previous sound-localization training in the conditioned-avoidance task. This difficulty suggested that the monkeys no longer associated the sound with a location in space. 4. The results of both the conditioned-avoidance and the two-choice tasks demonstrated that the animals were unable to discriminate the locus of a sound source when both loudspeakers were located in the same hemifield. 5. Bilateral ablation of auditory cortex results in both sensory and perceptual deficits. The presence of sensory deficits is indicated by the decreased acuity in the left-right discrimination and the inability to discriminate between two loudspeakers located in the same hemifield. The deficit in the perception of the locus of sound is indicated by the difficulty in learning to approach the source of a sound, an ability which normal monkeys exhibit without training. 6. There appear to be species' differences in the effect of auditory cortex lesions on sound localization. Although cortical lesions result in a sound-localization deficit in several species of primates and carnivores, they have little or no effect on rats.

Animals