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Perception of sounds used in species-specific communication: the auditory cortex and beyond.

The auditory cortex, located in the superior temporal gyrus, has been studied in squirrel monkeys with respect to its role in detecting species-specific vocalizations. Single neurons tested with selected vocalizations from the species' repertoire have been grouped into seven functional categories. Each category reflects a different level of processing with regard to vocalizations and artificial sounds. It is argued that, while the auditory cortex has the capability to detect and distinguish species-specific vocalizations, the interpretation of their biological significance likely takes place elsewhere.

Animal Communication

[The relationship between the second zone of the auditory cortex and the medial geniculate body and first auditory zone].

Extracellular and intracellular responses of the second auditory (AII) cortical neurons to stimulation of geniculocortical fibres and first auditory cortex (AI) were studied in experiments carried out on cats immobilized with d-tubocurarine. It is shown that in these neurons there appear antidromic, mono-, di- and polysynaptic spike potentials to geniculate and AI stimulation. The number of antidromic reactions was about twice as low as in AI under the same conditions. Di- and polysynaptic responses predominated among orthodromic reactions. Intracellular recording revealed EPSP, EPSP-IPSP and primary IPSP in AII neurons. Response latencies in AII neurons to AI stimulation were in the range of 0.75-6.0, 6.1-16.0, 18.0-23.0 and 60.100 ms. After the medial geniculate body was removed, the number of responses with a latency of 6.1-16.0 ms decreased considerably. In some neurons spike pontentials appeared both to geniculate and AI stimulation. Comparison of the response latencies at both types of stimulation showed that impulses from AI come in AII not only to the neurons that are inputs for MGB impulses but also to neurons in the sebsequent link of intracortical neuronal chain. In most AII neurons disynaptic IPSP appeared at AI stimulation. Only in one case IPSP with a latency of 1.0 ms was recorded being probably monosynaptic.

Animals

Contribution of auditory cortex to sound localization in the monkey (Macaca mulatta).

Monkeys with lesions of auditory cortex were tested for their ability to localize the source of brief sounds. Although those deprived of primary auditory cortex bilaterally were able to indicate the direction of a sound with near-normal acuity, they were unable to locate its source. This dissociation of abilities suggest that the role of auditory cortex in sound localization is not so much sensory or perceptual as it is auditomotor or associative. Thus, sound localization joins loudness, pitch, and most other traditional attributes of sound as dimensions whose discrimination does not depend on auditory cortex. The question would now seem to turn to whether or not auditory cortex is necessary for any sensory discrimination whatever.

Acoustic Stimulation

[After-discharges of cat auditory cortex neurons].

Afterdischarges in neurons of the auditory cortex (AI) were investigated in immobilized cats. The unit activity of 40% of neurons showed afterdischarges lasting 3--5 sec. after the cessation of the pure--tone or two--tone sound stimuli. Two--tone sound complexes consisted of the 1 st and higher harmonics with different phase relations between the components. The afterdischarges depended on some parameters of the sound stimuli. When tonal signal was used, 80% of neurons with obvious afterdischarges responded to the sound frequency. As regards the sensitivity to phase shifts in two--tone stimuli, changes of the activity occurred in 70% of cortical neurons with on-, off- and on--off reactions and were related to these components of the reaction. The pattern of afterdischarges in 19 of 32 neurons in the auditory cortex was also related to the phase shifts.

Action Potentials

Response variability in the mammalian auditory cortex: an objection to feature detection?

Research strategy in the auditory system has tended to parallel that in the visual system, where neurons have been shown to respond selectively to specific stimulus parameters. Auditory neurons have been shown to be sensitive to changes in acoustic parameters, but only rarely have neurons been reported that respond exclusively to only one biologically significant sound. Even at higher levels of the auditory system very few cells have been found that could be described as "vocalization detectors." In addition, variability in responses to artificial sounds have been reported for auditory cortical neurons similar to the response variability that has been reported in the visual system. Recent evidence indicates that the responses of auditory cortical neurons to species-specific vocalizations can also be labile, varying in both strength and selectivity. This is especially true of the secondary auditory cortex. This variability, coupled with the lack of extreme specificity in the secondary auditory cortex, suggests that secondary cortical neurons are not well suited for the role of "vocalization detectors."

Acoustic Stimulation

Auditory cortex lesions and discrimination of spatial location by the rat.

Five normal rats and four rats with bilateral lesions of auditory cortex were tested by the conditioned suppression procedure to determine their abilities to discriminate between spatially separated sound sources. The discrimination involved detection of a change in location of a train of clicks from a speaker on the animals' left to a speaker on the right. The separation between speakers was varied from 180 degrees to 90 degrees, 45 degrees, 22 degrees, 12 degrees, 6 degrees, and psychophysical functions were obtained using a method of descending limits. Both normal and brain-damaged animals were capable of discriminating left from right clicks and psychophysical curves were similar for the two groups. Histological analysis indicated that the lesions in each of the four brain-damaged rats destroyed primary auditory cortex as well as surrounding belt areas. Therefore, for the rat, auditory cortex was not found to be essential for discrimination of the spatial locations of auditory stimuli. The results are discussed in light of impairments in sound localization following lesions of auditory cortex in other mammalian species.

Acoustic Stimulation

Response plasticity of neurons in auditory cortex of the rhesus monkey.

Auditory-evoked responses in single neurons from rhesus monkey auditory cortex were measured under four relatively well defined behavioral and physiological conditions: (1) monkey awake and performing a simple auditory reaction time task; (2) monkey awake but not performing a task (Stage A); (3) monkey in a drowsy or Stage 1 sleep state (State B); and (4) monkey anesthetized with a short-acting nonbarbiturate anesthetic. For most units studied the response evoked by the auditory stimulus was greater in the performance condition than in the nonperformance condition. Similarly, evoked activity was usually greater in State A than in State B. Finally, evoked responses under anesthesia were usually weaker than those obtained in the unanesthetized animal. Some exceptions were noted in each case. Differences in response patterns and in rate versus intensity functions of neurons were also found to be associated with the behavioral and physiological state of the preparation. No significant changes in unit spontaneous activity associated with changes in behavioral or physiological condition were observed.

Acoustic Stimulation

Separate neuronal populations of the rat globus pallidus projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental area.

The topographic arrangement of globus pallidus neurons sending axons to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental nucleus was studied in the rat using retrograde fluorescent tracers. Neurons projecting to the subthalamic nucleus were localized in the rostral part of the globus pallidus, while neurons projecting to the auditory cortex and to the pedunculopontine tegmental nucleus were located in the caudal part. The two populations of pallidocortical and pallidotegmental neurons were also distributed in a separate manner within the caudal globus pallidus. The former neurons were large and located more ventromedially, whereas the latter were medium-sized and located more dorsolaterally. Using a retrograde fluorescent tracing technique combined with choline acetyltransferase immunofluorescence histochemistry, it was found that a vast majority of pallidocortical neurons expressed choline acetyltransferase immunoreactivity, and that pallidotegmental neurons rarely exhibited choline acetyltransferase immunoreactivity. A method of retrograde tracing with wheatgerm agglutinin conjugated with horseradish peroxidase associated to immunohistochemistry for glutamate decarboxylase confirmed the GABAergic nature of the pallidotegmental pathway. The present study revealed the independent nature of the globus pallidus neurons projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental nucleus. Within this cellular arrangement, the presence of functionally distinct neuronal populations at the caudal pallidal level was also identified, with large cholinergic cells innervating the neocortex and medium-sized GABAergic cells "feeding" the mesencephalic tegmentum.

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

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

[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

[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

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

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

[Role of the auditory cortex in animal recognition of synthesized vowels].

Discrimination of synthesized vowels [a] and [i] was studied in intact dogs and animals with an ablated auditory cortex. Electro-defensive and conditioned reflex methods were used. It has been found that as a result of learning an auditory image of a stationary vowel can be formed in intact dogs, which is invariant relatively to any change in the basic frequency of the voice, the intensity and duration of presentation (300 to 75 msec), and that two formants are sufficent for discrimination. The auditory image of the vowel is preserved after a bilateral ablation of the auditory cortical projection zone. Discrimination of vowels is disturbed in animals with a removed auditory cortex when information redundancy is reduced (diminished number of formants and reduced signal duration).

Animals

Proprioceptive effects on evoked responses to sounds in the cat auditory cortex.

With a view to analyse the influence of neck proprioceptors on directional hearing, evoked potentials (EPs) to dichotically or monaurally presented clicks were recorded from the auditory cortex of cats under deep Nembutal anaesthesia with their head pointing to the front, and then to the right or to the left side at 45 degrees. The change in the head position produced considerable changes in the amplitude of the two primary EP components and in their thresholds. The changes were of two kinds: either decrease or increase of the amplitude. At symmetrical points of the auditory cortex they went in the same direction. The also appeared in the associative zone with the same sign. With monaurally presented clicks, the change of the side of stimulation for the most part resulted in a reversal of the sign of the proprioceptive effect. Similar proprioceptive influences were recorded when the clicks were presented not through earphones but in an open acoustic field.

Animals