Integration of ascending and descending inputs in the auditory midbrain of anurans.

In anurans, the midbrain torus semicircularis is involved in auditory processing and audio-motor integration. In this study, we examined the influence of descending forebrain projections on the auditory response properties and hence the audiomotor transmission of mesencephalic interface neurons. In order to investigate response integration, we performed intracellular recordings from torus neurons in an isolated brain preparation of Discoglossus pictus and Bombina orientalis and stimulated the auditory nerve, striatum, and the dorsal thalamus electrically with single pulses. Stimulation of all three sites could evoke responses in torus neurons that were either excitatory, inhibitory, or a mixture of both, with durations of up to several hundred milliseconds. Further, striatum and thalamus were activated by pulse trains (10-20 Hz, 50 pulses) immediately before stimulating the auditory nerve with single pulses. Thus, responses of torus neurons to "auditory" input were facilitated or suppressed for up to 2 min by striatum stimulation or only suppressed by thalamus stimulation. Intracellular labeling of recorded neurons revealed that response modulation by descending input mostly occurred in laminar nucleus neurons. These results suggest that descending forebrain projections to mesencephalic audiomotor interface neurons may play an important role in modifying acoustically guided behavior in anurans.     

Efferent neurons of the auditory center in the midbrain of the frog Rana ridibunda

Individual cells which produce projections from the torus semicircularis in the frog have been visualized after injection of horseradish peroxidase (HRP) to various thalamic and isthmal areas. Labeled toral cells were observed if HRP had been injected to the posterodorsal areas of the thalamus or to the isthmal areas where lateral lemniscus fibers and cells of the premature lateral lemniscal nucleus are situated. Medium and large size cells in the rostrolateral torus semicircularis were mainly labeled. Thalamic injections of the HRP produced more labeled cells in the lateral part of the magnocellular nucleus, whereas isthmal injections produced labeled cells mainly in the lateral part of the laminar nucleus. A few HRP containing cells were observed in the principal nucleus of the torus. Specificity of the neuronal organisation of the auditory pathway in amphibians is discussed.     

Common system of sparsely branched projection (reticular) NADPH-diaphorase neurons in the human forebrain formations built from densely branched cells

Cell morphometry with statistical analysis (using 9 parameters) of densely branched projection and sparsely branched reticular neurons was performed in the human forebrain formations built from densely branched projection neurons (the entorhinal cortex, striatum, nucleus accumbens basolateral amygdala, and dorsal thalamus). The reticular neurons included scattered reticular neurons and marginal reticular neurons of the dorsal thalamus. Golgi method and staining for NADPH-diaphorase were used. The scattered reticular neurons of different formations under study did not differ in any of the 9 parameters, whereas they significantly differed from the main projection neurons in 5 to 7 parameters (except one comparison with the difference in 2 parameters). Within the same formation, the scattered reticular and main projection densely branched neurons differed in 7 to 9 parameters. The endbrain scattered reticular neurons expressed NADPH-diaphorase, while in the dorsal thalamus only the medium marginal reticular neurons were NADPH-diaphorase-positive. Thus, a common system of ancient integrative reticular neurons expressing NADPH-diaphorase exists in the examined human forebrain formations. The evidence obtained by us and the literature data point to the projection nature of the scattered reticular neurons (to the V and VI neocortical layers), which suggests their modulatory influence on descending neocortical pathways.     

Rapid effects of hearing song on catecholaminergic activity in the songbird auditory pathway

Catecholaminergic (CA) neurons innervate sensory areas and affect the processing of sensory signals. For example, in birds, CA fibers innervate the auditory pathway at each level, including the midbrain, thalamus, and forebrain. We have shown previously that in female European starlings, CA activity in the auditory forebrain can be enhanced by exposure to attractive male song for one week. It is not known, however, whether hearing song can initiate that activity more rapidly. Here, we exposed estrogen-primed, female white-throated sparrows to conspecific male song and looked for evidence of rapid synthesis of catecholamines in auditory areas. In one hemisphere of the brain, we used immunohistochemistry to detect the phosphorylation of tyrosine hydroxylase (TH), a rate-limiting enzyme in the CA synthetic pathway. We found that immunoreactivity for TH phosphorylated at serine 40 increased dramatically in the auditory forebrain, but not the auditory thalamus and midbrain, after 15 min of song exposure. In the other hemisphere, we used high pressure liquid chromatography to measure catecholamines and their metabolites. We found that two dopamine metabolites, dihydroxyphenylacetic acid and homovanillic acid, increased in the auditory forebrain but not the auditory midbrain after 30 min of exposure to conspecific song. Our results are consistent with the hypothesis that exposure to a behaviorally relevant auditory stimulus rapidly induces CA activity, which may play a role in auditory responses.     

Distribution of GABA-immunoreactive neurons in the brain of adult and developing salamanders (Pleurodeles waltli,Triturus alpestris)

The distribution of GABAergic neurons in brains of the family Salamandridae (Pleurodeles waltli, Triturus alpestris) has been investigated immunohistochemically with an antibody against gamma-aminobutyric acid (GABA). In adult animals, immunoreactive neurons, fibers, and terminals are abundantly labeled. In the telencephalon, pallial areas contain fewer GABAergic neurons and fibers than basal forebrain areas. The amygdalar complex and the habenulae have a complex pattern of GABA-immunoreactivity that is especially pronounced within the neuropil. The pretectal and basal optic systems are provided with GABAergic neurons, corroborating electrophysiological results. The dorsal thalamus and parts of the torus semicircularis are almost completely devoid of GABA-immunoreactive neurons. In the torus, magnocellular neurons known to project to the contralateral counterpart are distinctly GABA-immunoreactive. During ontogeny, GABAergic neurons arise early when the first reflexive movements occur after mechanical stimulation. At stage 28, cells are labeled initially near the nucleus of the medial longitudinal fasciculus, which is the first supraspinal tract to appear in ontogeny. At stage 30 (still before hatching), GABAergic neurons are found in the pretectum, immunoreactive neurons arising in the dorsal tegmentum slightly later. Both systems are known to mediate basic reflexes in gaze stabilization. The commissura posterior is GABAergic at early stages suggesting an important functional role in homonymous inhibition between both sides. Thus in salamanders, the neurotransmitter GABA displays a complex distribution, similar to that in other vertrebrates. This pattern emerges early in ontogeny.     

Gonadotropin-releasing hormone (GnRH) modulates auditory processing in the fish brain

Gonadotropin-releasing hormone 1 (GnRH1) neurons control reproductive activity, but GnRH2 and GnRH3 neurons have widespread projections and function as neuromodulators in the vertebrate brain. While these extra-hypothalamic GnRH forms function as olfactory and visual neuromodulators, their potential effect on processing of auditory information is unknown. To test the hypothesis that GnRH modulates the processing of auditory information in the brain, we used immunohistochemistry to determine seasonal variations in these neuropeptide systems, and in vivo single-neuron recordings to identify neuromodulation in the midbrain torus semicircularis of the soniferous damselfish Abudefduf abdominalis. Our results show abundant GnRH-immunoreactive (-ir) axons in auditory processing regions of the midbrain and hindbrain. The number of extra-hypothalamic GnRH somata and the density of GnRH-ir axons within the auditory torus semicircularis also varied across the year, suggesting seasonal changes in GnRH influence of auditory processing. Exogenous application of GnRH (sGnRH and cGnRHII) caused a primarily inhibitory effect on auditory-evoked single neuron responses in the torus semicircularis. In the majority of neurons, GnRH caused a long-lasting decrease in spike rate in response to both tone bursts and playbacks of complex natural sounds. GnRH also decreased response latency and increased auditory thresholds in a frequency and stimulus type-dependent manner. To our knowledge, these results show for the first time in any vertebrate that GnRH can influence context-specific auditory processing in vivo in the brain, and may function to modulate seasonal auditory-mediated social behaviors.     

The cytoarchitecture of the torus semicircularis in the golden skink Mabuya multifasciata

The skink, Mabuya multifasciata, torus semicircularis was subdivided into the central (CN), the laminar (LN), and the superficial (SN) nuclei using Golgi and Nissl methods. The central nucleus consisted of small ovoid neurons surrounding a core of fewer large ovoid-triangular and fusiform neurons. The ovoid cells had scant cytoplasm and two to five dendritic trunks. Most of these processes were directed around the periphery of the central nucleus. The large neurons had clumped, darkly staining Nissl substance and a central nucleus. The sparse dendritic spine population on these cells increased distally on the three to five radiate dendrites. The laminar nucleus was present caudal and ventral to the central nucleus. At more rostral levels it was medial and dorsomedial to the central nucleus. The NL had three to five layers of ovoid and fusiform neurons. Scattered within these layers were a few ovoid-triangular neurons. Ovoid neurons had eccentric or central nuclei. The arborization of their dendrites was generally medial and lateral but was frequently oriented caudomedial and rostrolateral. Fusiform neurons had pale Nissl substance, central nuclei, and one to two dendritic processes. The ovoid-triangular neurons had dense, clumped Nissl substance and at least two dendritic trunks with few spines. The superficial nucleus was dorsal, lateral, and caudal to the central nucleus. Extending ventrolaterally around the central nucleus, the superficial nucleus became confluent with the laminar nucleus, ensheathing the central nucleus ventrally, laterally, and dorsally. Rostrally the central nucleus was covered by the layers of the laminar nucleus. Within the superficial nucleus were ovoid, fusiform and sparse ovoid-triangular neurons. The study indicated that the morphology of the torus semicircularis in the golden skink was similar to that in other lizards. This similarity correlates with the degree of development as it relates to the auditory function, but was independent of the type of inner ear restraint mechanism.     

Morphology of neurons and axon terminals associated with descending and ascending pathways of the lateral forebrain bundle in Rana esculenta

Summary The cells of origin of afferent and efferent pathways of the lateral forebrain bundle were studied with the aid of the cobalt-filling technique. Ascending afferents originated from the lateral thalamic nucleus, central thalamic nucleus, posterior tuberculum and the cerebellar nucleus. They terminated in the anterior entopeduncular nucleus, amygdala and the striatum. Telencephalic projection neurons, which are related to the lateral forebrain bundle, were located mainly in the ventral striatum and the anterior entopeduncular nucleus, but were not so numerous in the dorsal striatum. Irrespective of their location, most of the neurons projecting axons into the lateral forebrain bundle had piriform or pyramidal perikarya. Long apical dendrites usually arborized in a narrow space, whereas widely arborizing secondary dendrites originated from short dendritic trunks. The other neurons that contributed to the lateral forebrain bundle were fusiform or multipolar cells. Striatal efferents terminated in the pretectal area and in the anterodorsal, anteroventral and posteroventral tegmental nuclei.     

The torus semicircularis in a gekkonid lizard

The cytoarchitecture and neuromorphology of the torus semicircularis in the tokay gecko, Gekko gecko, were examined in Nissl-stained, fiber-stained, and Golgi-impregnated tissues. From a superficial position, the torus semicircularis extends rostrally under the caudal half of the optic tectum. Caudally, the two tori abut upon one another; rostrally, they diverge. The torus semicircularis consists of central, laminar, and superficial nuclei. The central nucleus consists of fusiform, spherical and triangular neurons. Their dendrites are highly branched, with numerous dendritic spines, and are oriented mediolaterally, dorsoventrally, and rostrocaudally. Fusiform and spherical neurons display two dendritic patterns: “single axis,” ramifying in one axis, and “dual axis,” exhibiting higher-order branches perpendicular to the primary dendrites. Triangular neurons exhibit a “radiate” dendritic pattern. In the rostral half of the torus semicircularis, the laminar nucleus caps the central nucleus. The laminar nucleus encircles the central nucleus in the caudal torus semicircularis. The neurons of the laminar nucleus have dendritic arrays oriented parallel to the border of the central nucleus. These dendrites exhibit a paucity of dendritic spines and higher-order branches. Fusiform and spherical neurons exhibit “single axis” and “dual axis” dendritic patterns. Triangular neurons display “radiate” patterns. The caudal superficial nucleus lies dorsal and dorsolateral to the central nucleus. The superficial nucleus is sparsely populated by small fusiform and spherical neurons with moderately branched dendrites and moderate numbers of dendritic spines. These neurons display “single axis” (fusiform neurons) as well as “dual axis” and “radiate” (spherical neurons) dendritic patterns. They are oriented either parallel to or perpendicular to the boundary of the laminar nucleus.     

Emergence of tuning to natural stimulus statistics along the central auditory pathway

We have previously shown that neurons in primary auditory cortex (A1) of anaesthetized (ketamine/medetomidine) ferrets respond more strongly and reliably to dynamic stimuli whose statistics follow "natural" 1/f dynamics than to stimuli exhibiting pitch and amplitude modulations that are faster (1/f(0.5)) or slower (1/f(2)) than 1/f. To investigate where along the central auditory pathway this 1/f-modulation tuning arises, we have now characterized responses of neurons in the central nucleus of the inferior colliculus (ICC) and the ventral division of the mediate geniculate nucleus of the thalamus (MGV) to 1/f(γ) distributed stimuli with γ varying between 0.5 and 2.8. We found that, while the great majority of neurons recorded from the ICC showed a strong preference for the most rapidly varying (1/f(0.5) distributed) stimuli, responses from MGV neurons did not exhibit marked or systematic preferences for any particular γ exponent. Only in A1 did a majority of neurons respond with higher firing rates to stimuli in which γ takes values near 1. These results indicate that 1/f tuning emerges at forebrain levels of the ascending auditory pathway.     

Tegmento-telencephalic relations in turtles

Electrophysiological characteristics of tegmental projections in the forebrain were studied in immobilized turtles (Emys orbicularis), anesthetized with chloralose. The main zone of representation of the tegmentum is located in the striatum, where evoked responses with shorter latencies were recorded and a larger number of units responding distinctly to tegmental stimulation was concentrated than in the dorsal ventricular ridge and general cortex. At the striatal level predominance of lateral tegmental projections was found in the lateral zone and of medial tegmental projections in the medial zone of the striatum. An inhibitory action of conditioning stimulation of the tegmentum on somatic evoked potentials and single unit responses was established. An attempt was made to compare the tegmento-telencephalic system in reptiles and mammals.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 12, No. 3, pp. 255–263, May–June, 1980.     

Morphological and physiological study of afferent projections of the posterolateral thalamic nucleus in rats

It was shown by the method of retrograde axonal transport of horseradish peroxidase that the posterolateral thalamic nucleus (NPL) in rats receives considerable ascending projections from the superior colliculus (SC), the dorsal part of the lateral geniculate body (LGB), and the pretectal region (PT) and smaller projections from n. ventralis posterior (VP) and n. ventralis lateralis (VL) of the thalamus, the ventral part of LGB, the zona incerta, and anterior hypothalamus. The most marked descending projections run into NPL from area 18A of the cortex and the dentate fascia of the hippocampus, whereas inputs from cortical areas 18, 20, 7, 29c, 17, and 36 are less marked. In electrophysiological experiments with peripheral stimulation of visual, auditory, and somatosensory systems, polysensory convergence and interaction between signals from these systems were studied during isolated and simultaneous presentation of heterosensory stimuli. Of 229 neurons tested, 134 (58.5%) responded to at least one of the stimuli mentioned. Among monomodal neurons (53 of 134) there were some cells which responded to visual (77.4%) and somatic (22.6%) stimulation; neurons which responded only to acoustic stimulation were not found in the nucleus. As far as polymodal neurons (81 of 134) responding to two or three sensory stimuli are concerned, the most effective inputs of these units were visual and somatosensory. Interaction between stimuli acting on polymodal neurons was expressed as mutual inhibition or facilitation of responses; opposite effects could be observed on the various components of these responses.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 16, No. 2, pp. 168–176, March–April, 1984.     

Axonal conduction properties of antidromically identified neurons in rat barrel cortex

Physiological studies of the rodent somatosensory cortex have consistently described considerable heterogeneity in receptive field properties of neurons outside of layer IV, particularly those in layers V and VI. One such approach for distinguishing among different local circuits in these layers may be to identify the projection target of neurons whose axon collaterals contribute to the local network. In vivo, this can be accomplished using antidromic stimulation methods. Using this approach, the axonal conduction properties of cortical efferent neurons are described. Four projection sites were activated using electrical stimulation: (1) vibrissal motor cortex, (2) ventrobasal thalamus (VB), (3) posteromedial thalamic nucleus (POm), and (4) cerebral peduncle. Extracellular recordings were obtained from a total of 169 units in 21 animals. Results demonstrate a close correspondence between the laminar location of the antidromically identified neurons and their anatomically known layer of origin. Axonal properties were most distinct for corticofugal axons projecting through the crus cerebri. Corticothalamic axons projecting to either VB or POm were more similar to each other in terms of laminar location and conduction properties, but could be distinguished using focal electrical stimulation. It is concluded that, once stimulation parameters are adjusted for the small volume of the rat brain, the use of antidromic techniques may be an effective strategy to differentiate among projection neurons comprising different local circuits in supra- and infragranular circuits.     

Corticofugal modulation of initial neural processing of sound information from the ipsilateral ear in the mouse

Background

Cortical neurons implement a high frequency-specific modulation of subcortical nuclei that includes the cochlear nucleus. Anatomical studies show that corticofugal fibers terminating in the auditory thalamus and midbrain are mostly ipsilateral. Differently, corticofugal fibers terminating in the cochlear nucleus are bilateral, which fits to the needs of binaural hearing that improves hearing quality. This leads to our hypothesis that corticofugal modulation of initial neural processing of sound information from the contralateral and ipsilateral ears could be equivalent or coordinated at the first sound processing level.

Methodology/Principal Findings

With the focal electrical stimulation of the auditory cortex and single unit recording, this study examined corticofugal modulation of the ipsilateral cochlear nucleus. The same methods and procedures as described in our previous study of corticofugal modulation of contralateral cochlear nucleus were employed simply for comparison. We found that focal electrical stimulation of cortical neurons induced substantial changes in the response magnitude, response latency and receptive field of ipsilateral cochlear nucleus neurons. Cortical stimulation facilitated auditory response and shortened the response latency of physiologically matched neurons whereas it inhibited auditory response and lengthened the response latency of unmatched neurons. Finally, cortical stimulation shifted the best frequencies of cochlear neurons towards those of stimulated cortical neurons.

Conclusion

Our data suggest that cortical neurons enable a high frequency-specific remodelling of sound information processing in the ipsilateral cochlear nucleus in the same manner as that in the contralateral cochlear nucleus.     

Connections between the anterior thalamic nuclei in turtles (data of the peroxidase method)

It turtles, Testudo horsfieldi (Gray) connections of anterior dorsomedial and dorsolateral thalamic nuclei have been investigated by means of horseradish peroxidase, injected ionophoretically. Retrogradely labelled neurons are predominantly revealed ipsilaterally in the cerebral structures belonging to the limbic system: in the forebrain--basal parts of the hemisphere, septum, adjoining nucleus, nuclei of the anterior and hippocampal commissures, hippocampal cortex, preoptic area; in the diencephalon--in the subthalamus (suprapeduncular nucleus), in some hypothalamic structures (para- and periventricular nuclei, posterior nucleus, lateral hypothalamic area, mamillary complex); in the brain stem--ventral tegmental area, superior nucleus of the suture. Less vast connections are with nonlimbic cerebral formations: projections to the striatum, afferents from the laminar nucleus of the acoustic torus, nuclei of the posterior commissure. Similarity and difference of the nuclei investigated in the turtles with the thalamic anterior nuclei in lizards, with the anterior and intralaminar nuclei in Mammalia are discussed. An idea is suggested on functional heterogeneity of the anterior nuclei in reptiles and on their role for ensuring limbic functions at the thalamic level.     

Testosterone alters genomic responses to song and monoaminergic innervation of auditory areas in a seasonally breeding songbird

Behavioral responses to social stimuli often vary according to endocrine state. Our previous work has suggested that such changes in behavior may be due in part to hormone‐dependent sensory processing. In the auditory forebrain of female white‐throated sparrows, expression of the immediate early gene ZENK (egr‐1) is higher in response to conspecific song than to a control sound only when plasma estradiol reaches breeding‐typical levels. Estradiol also increases the number of detectable noradrenergic neurons in the locus coeruleus and the density of noradrenergic and serotonergic fibers innervating auditory areas. We hypothesize, therefore, that reproductive hormones alter auditory responses by acting on monoaminergic systems. This possibility has not been examined in males. Here, we treated non‐breeding male white‐throated sparrows with testosterone to mimic breeding‐typical levels and then exposed them to conspecific male song or frequency‐matched tones. We observed selective ZENK responses in the caudomedial nidopallium only in the testosterone‐treated males. Responses in another auditory area, the caudomedial mesopallium, were selective regardless of hormone treatment. Testosterone treatment reduced serotonergic fiber density in the auditory forebrain, thalamus, and midbrain, and although it increased the number of noradrenergic neurons detected in the locus coeruleus, it reduced noradrenergic fiber density in the auditory midbrain. Thus, whereas we previously reported that estradiol enhances monoaminergic innervation of the auditory pathway in females, we show here that testosterone decreases it in males. Mechanisms underlying testosterone‐dependent selectivity of the ZENK response may differ from estradiol‐dependent ones.© 2013 Wiley Periodicals, Inc. Develop Neurobiol 73: 455–468, 2013     

The hypocretin neuron system: an arousal system in the human brain

Hypocretins are recently discovered neuropeptides produced by a small group of posterior hypothalamic neurons which project widely over the neuroaxis. In this study, we note that hypocretin neuron perikarya in the human brain are localized to the perifornical region of the posterior hypothalamus, extending into the lateral hypothalamus. These neurons lightly innervate all areas of cerebral cortex studied in a variable pattern with denser innervation of association cortex than primary motor or sensory cortex. There is a dense innervation of hypothalamus, locus coeruleus, raphe nuclei, midline thalamus and nucleus of the diagonal band-nucleus basalis complex of the forebrain. This pattern of projections from the hypocretin neurons is compatible with an important role in arousal and the maintenance of the waking state.     

Sexually dimorphic androgen and estrogen receptor mRNA expression in the brain of túngara frogs

Sex steroid hormones are potent regulators of behavior and they exert their effects through influences on sensory, motor, and motivational systems. To elucidate where androgens and estrogens can act to regulate sex-typical behaviors in the túngara frog (Physalaemus pustulosus), we quantified expression of the androgen receptor (AR), estrogen receptor alpha (ERα), and estrogen receptor beta (ERβ) genes in the brains of male and females. To do so, we cloned túngara-specific sequences for AR, ERα, and ERβ, determined their distribution in the brain, and then quantified their expression in areas that are important in sexual communication. We found that AR, ERα, and ERβ were expressed in the pallium, limbic forebrain (preoptic area, hypothalamus, nucleus accumbens, amygdala, septum, striatum), parts of the thalamus, and the auditory midbrain (torus semicircularis). Males and females had a similar distribution of AR and ER expression, but expression levels differed in some brain regions. In the auditory midbrain, females had higher ERα and ERβ expression than males, whereas males had higher AR expression than females. In the forebrain, females had higher AR expression than males in the ventral hypothalamus and medial pallium (homolog to hippocampus), whereas males had higher ERα expression in the medial pallium. In the preoptic area, striatum, and septum, males and females had similar levels of AR and ER expression. Our results suggest that sex steroid hormones have sexually dimorphic effects on auditory processing, sexual motivation, and possibly memory and, therefore, have important implications for sexual communication in this system.     

Role of corticofugal feedback in hearing

The auditory system consists of the ascending and descending (corticofugal) systems. The corticofugal system forms multiple feedback loops. Repetitive acoustic or auditory cortical electric stimulation activates the cortical neural net and the corticofugal system and evokes cortical plastic changes as well as subcortical plastic changes. These changes are short-term and are specific to the properties of the acoustic stimulus or electrically stimulated cortical neurons. These plastic changes are modulated by the neuromodulatory system. When the acoustic stimulus becomes behaviorally relevant to the animal through auditory fear conditioning or when the cortical electric stimulation is paired with an electric stimulation of the cholinergic basal forebrain, the cortical plastic changes become larger and long-term, whereas the subcortical changes stay short-term, although they also become larger. Acetylcholine plays an essential role in augmenting the plastic changes and in producing long-term cortical changes. The corticofugal system has multiple functions. One of the most important functions is the improvement and adjustment (reorganization) of subcortical auditory signal processing for cortical signal processing.