It has long been known that environmental conditions, particularly during development, affect morphological and functional properties of the brain including sensory systems; manipulating the environment thus represents a viable way to explore experience-dependent plasticity of the brain as well as of sensory systems. In this review, we summarize our experience with the effects of acoustically enriched environment (AEE) consisting of spectrally and temporally modulated complex sounds applied during first weeks of the postnatal development in rats and compare it with the related knowledge from the literature. Compared to controls, rats exposed to AEE showed in neurons of several parts of the auditory system differences in the dendritic length and in number of spines and spine density. The AEE exposure permanently influenced neuronal representation of the sound frequency and intensity resulting in lower excitatory thresholds, increased frequency selectivity and steeper rate-intensity functions. These changes were present both in the neurons of the inferior colliculus and the auditory cortex (AC). In addition, the AEE changed the responsiveness of AC neurons to frequency modulated, and also to a lesser extent, amplitude-modulated stimuli. Rearing rat pups in AEE leads to an increased reliability of acoustical responses of AC neurons, affecting both the rate and the temporal codes. At the level of individual spikes, the discharge patterns of individual neurons show a higher degree of similarity across stimulus repetitions. Behaviorally, rearing pups in AEE resulted in an improvement in the frequency resolution and gap detection ability under conditions with a worsened stimulus clarity. Altogether, the results of experiments show that the exposure to AEE during the critical developmental period influences the frequency and temporal processing in the auditory system, and these changes persist until adulthood. The results may serve for interpretation of the effects of the application of enriched acoustical environment in human neonatal medicine, especially in the case of care for preterm born children.
- Klíčová slova
- Acoustically enriched environment, Auditory system, Critical period, Development, Plasticity,
- MeSH
- akustická stimulace * MeSH
- akustika MeSH
- colliculus inferior růst a vývoj fyziologie MeSH
- krysa rodu Rattus MeSH
- lidé MeSH
- neurony fyziologie MeSH
- neuroplasticita * fyziologie MeSH
- novorozená zvířata MeSH
- sluchová dráha * růst a vývoj fyziologie MeSH
- sluchová percepce MeSH
- sluchové korové centrum * růst a vývoj fyziologie MeSH
- věkové faktory MeSH
- životní prostředí MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
The LIM homeodomain transcription factor ISL1 is essential for the different aspects of neuronal development and maintenance. In order to study the role of ISL1 in the auditory system, we generated a transgenic mouse (Tg) expressing Isl1 under the Pax2 promoter control. We previously reported a progressive age-related decline in hearing and abnormalities in the inner ear, medial olivocochlear system, and auditory midbrain of these Tg mice. In this study, we investigated how Isl1 overexpression affects sound processing by the neurons of the inferior colliculus (IC). We recorded extracellular neuronal activity and analyzed the responses of IC neurons to broadband noise, clicks, pure tones, two-tone stimulation and frequency-modulated sounds. We found that Tg animals showed a higher inhibition as displayed by two-tone stimulation; they exhibited a wider dynamic range, lower spontaneous firing rate, longer first spike latency and, in the processing of frequency modulated sounds, showed a prevalence of high-frequency inhibition. Functional changes were accompanied by a decreased number of calretinin and parvalbumin positive neurons, and an increased expression of vesicular GABA/glycine transporter and calbindin in the IC of Tg mice, compared to wild type animals. The results further characterize abnormal sound processing in the IC of Tg mice and demonstrate that major changes occur on the side of inhibition.
- Klíčová slova
- auditory system, inferior colliculus, inhibition, sound processing, transcription factor ISL1,
- MeSH
- colliculus inferior metabolismus fyziologie MeSH
- exprese genu genetika MeSH
- lidé MeSH
- mozek fyziologie MeSH
- myši transgenní MeSH
- myši MeSH
- neurony fyziologie MeSH
- promotorové oblasti (genetika) genetika MeSH
- proteiny s homeodoménou LIM genetika metabolismus MeSH
- sluch MeSH
- sluchová percepce genetika fyziologie MeSH
- sluchové kmenové evokované potenciály fyziologie MeSH
- sluchový práh fyziologie MeSH
- transkripční faktor PAX2 genetika MeSH
- transkripční faktory genetika metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- mužské pohlaví MeSH
- myši MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- insulin gene enhancer binding protein Isl-1 MeSH Prohlížeč
- PAX2 protein, human MeSH Prohlížeč
- Pax2 protein, mouse MeSH Prohlížeč
- proteiny s homeodoménou LIM MeSH
- transkripční faktor PAX2 MeSH
- transkripční faktory MeSH
The structure of neurons in the central auditory system is vulnerable to various kinds of acoustic exposures during the critical postnatal developmental period. Here we explored long-term effects of exposure to an acoustically enriched environment (AEE) during the third and fourth weeks of the postnatal period in rat pups. AEE consisted of a spectrally and temporally modulated sound of moderate intensity, reinforced by a behavioral paradigm. At the age of 3-6 months, a Golgi-Cox staining was used to evaluate the morphology of neurons in the inferior colliculus (IC), the medial geniculate body (MGB), and the auditory cortex (AC). Compared to controls, rats exposed to AEE showed an increased mean dendritic length and volume and the soma surface in the external cortex and the central nucleus of the IC. The spine density increased in both the ventral and dorsal divisions of the MGB. In the AC, the total length and volume of the basal dendritic segments of pyramidal neurons and the number and density of spines on these dendrites increased significantly. No differences were found on apical dendrites. We also found an elevated number of spines and spine density in non-pyramidal neurons. These results show that exposure to AEE during the critical developmental period can induce permanent changes in the structure of neurons in the central auditory system. These changes represent morphological correlates of the functional plasticity, such as an improvement in frequency tuning and synchronization with temporal parameters of acoustical stimuli.
- Klíčová slova
- Central auditory system, Critical period, Dendrites, Enriched environment, Rat, Spines,
- MeSH
- akustická stimulace MeSH
- colliculus inferior cytologie fyziologie MeSH
- dendritické trny fyziologie MeSH
- dendrity fyziologie MeSH
- krysa rodu Rattus MeSH
- metathalamus cytologie fyziologie MeSH
- neurony cytologie fyziologie MeSH
- neuroplasticita fyziologie MeSH
- novorozená zvířata MeSH
- potkani Long-Evans MeSH
- sluchová dráha cytologie fyziologie MeSH
- sluchové korové centrum cytologie fyziologie MeSH
- tvar buňky fyziologie MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
To examine whether exposure to sodium salicylate disrupts expression of vesicular glutamate transporter 3 (VGLUT3) and whether the alteration in expression corresponds to increased risk for tinnitus. Rats were treated with saline (control) or sodium salicylate (treated) Rats were examined for tinnitus by monitoring gap-pre-pulse inhibition of the acoustic startle reflex (GPIAS). Auditory brainstem response (ABR) was applied to evaluate hearing function after treatment. Rats were sacrificed after injection to obtain the cochlea, cochlear nucleus (CN), and inferior colliculus (IC) for examination of VGLUT3 expression. No significant differences in hearing thresholds between groups were identified (p>0.05). Tinnitus in sodium salicylate-treated rats was confirmed by GPIAS. VGLUT3 encoded by solute carrier family 17 members 8 (SLC17a8) expression was significantly increased in inner hair cells (IHCs) of the cochlea in treated animals, compared with controls (p<0.01). No significant differences in VGLUT3 expression between groups were found for the cochlear nucleus (CN) or IC (p>0.05). Exposure to sodium salicylate may disrupt SLC17a8 expression in IHCs, leading to alterations that correspond to tinnitus in rats. However, the CN and IC are unaffected by exposure to sodium salicylate, suggesting that enhancement of VGLUT3 expression in IHCs may contribute to the pathogenesis of tinnitus.
- MeSH
- antiflogistika nesteroidní škodlivé účinky MeSH
- colliculus inferior účinky léků metabolismus MeSH
- nucleus cochlearis účinky léků metabolismus MeSH
- potkani Wistar MeSH
- salicylan sodný škodlivé účinky MeSH
- sluchový práh účinky léků MeSH
- tinnitus chemicky indukované MeSH
- vezikulární transportní proteiny pro glutamát metabolismus MeSH
- vnitřní vláskové buňky účinky léků metabolismus MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antiflogistika nesteroidní MeSH
- salicylan sodný MeSH
- Slc17a8 protein, rat MeSH Prohlížeč
- vezikulární transportní proteiny pro glutamát MeSH
When modeling auditory responses to environmental sounds, results are satisfactory if both training and testing are restricted to datasets of one type of sound. To predict 'cross-sound' responses (i.e., to predict the response to one type of sound e.g., rat Eating sound, after training with another type of sound e.g., rat Drinking sound), performance is typically poor. Here we implemented a novel approach to improve such cross-sound modeling (single unit datasets were collected at the auditory midbrain of anesthetized rats). The method had two key features: (a) population responses (e.g., average of 32 units) instead of responses of individual units were analyzed; and (b) the long sound segment was first divided into short segments (single sound-bouts), their similarity was then computed over a new metric involving the response (called Stimulus Response Model map or SRM map), and finally similar sound-bouts (regardless of sound type) and their associated responses (peri-stimulus time histograms, PSTHs) were modelled. Specifically, a committee machine model (artificial neural networks with 20 stratified spectral inputs) was trained with datasets from one sound type before predicting PSTH responses to another sound type. Model performance was markedly improved up to 92%. Results also suggested the involvement of different neural mechanisms in generating the early and late responses to amplitude transients in the broad-band environmental sounds. We concluded that it is possible to perform rather satisfactory cross-sound modeling on datasets grouped together based on their similarities in terms of the new metric of SRM map.
- Klíčová slova
- Artificial neural network, Complex sound processing, Cross-sound modeling, Inferior colliculus, Rat,
- MeSH
- akustická stimulace metody MeSH
- biologické modely * MeSH
- colliculus inferior fyziologie MeSH
- krysa rodu Rattus MeSH
- neuronové sítě * MeSH
- neurony fyziologie MeSH
- potkani Sprague-Dawley MeSH
- sluchové kmenové evokované potenciály fyziologie MeSH
- systémová biologie MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Hearing depends on extracting frequency, intensity, and temporal properties from sound to generate an auditory map for acoustical signal processing. How physiology intersects with molecular specification to fine tune the developing properties of the auditory system that enable these aspects remains unclear. We made a novel conditional deletion model that eliminates the transcription factor NEUROD1 exclusively in the ear. These mice (both sexes) develop a truncated frequency range with no neuroanatomically recognizable mapping of spiral ganglion neurons onto distinct locations in the cochlea nor a cochleotopic map presenting topographically discrete projections to the cochlear nuclei. The disorganized primary cochleotopic map alters tuning properties of the inferior colliculus units, which display abnormal frequency, intensity, and temporal sound coding. At the behavioral level, animals show alterations in the acoustic startle response, consistent with altered neuroanatomical and physiological properties. We demonstrate that absence of the primary afferent topology during embryonic development leads to dysfunctional tonotopy of the auditory system. Such effects have never been investigated in other sensory systems because of the lack of comparable single gene mutation models.SIGNIFICANCE STATEMENT All sensory systems form a topographical map of neuronal projections from peripheral sensory organs to the brain. Neuronal projections in the auditory pathway are cochleotopically organized, providing a tonotopic map of sound frequencies. Primary sensory maps typically arise by molecular cues, requiring physiological refinements. Past work has demonstrated physiologic plasticity in many senses without ever molecularly undoing the specific mapping of an entire primary sensory projection. We genetically manipulated primary auditory neurons to generate a scrambled cochleotopic projection. Eliminating tonotopic representation to auditory nuclei demonstrates the inability of physiological processes to restore a tonotopic presentation of sound in the midbrain. Our data provide the first insights into the limits of physiology-mediated brainstem plasticity during the development of the auditory system.
- Klíčová slova
- Neurod1 mutation, auditory pathway, cochlear nucleus, inferior colliculus, plasticity, sensory topographical map,
- MeSH
- chování zvířat fyziologie MeSH
- colliculus inferior anatomie a histologie fyziologie MeSH
- ganglion spirale cytologie fyziologie MeSH
- mapování mozku MeSH
- mezencefalon embryologie fyziologie MeSH
- myši knockoutované MeSH
- myši MeSH
- nucleus cochlearis anatomie a histologie fyziologie MeSH
- sluch fyziologie MeSH
- sluchová percepce genetika fyziologie MeSH
- těhotenství MeSH
- transkripční faktory bHLH genetika fyziologie MeSH
- úleková reakce genetika fyziologie MeSH
- vestibulární aparát anatomie a histologie fyziologie MeSH
- vnímání výšky zvuku fyziologie MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- myši MeSH
- těhotenství MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- Neurod1 protein, mouse MeSH Prohlížeč
- transkripční faktory bHLH MeSH
For all sensory organs, the establishment of spatial and temporal cortical resolution is assumed to be initiated by the first sensory experience and a BDNF-dependent increase in intracortical inhibition. To address the potential of cortical BDNF for sound processing, we used mice with a conditional deletion of BDNF in which Cre expression was under the control of the Pax2 or TrkC promoter. BDNF deletion profiles between these mice differ in the organ of Corti (BDNF (Pax2) -KO) versus the auditory cortex and hippocampus (BDNF (TrkC) -KO). We demonstrate that BDNF (Pax2) -KO but not BDNF (TrkC) -KO mice exhibit reduced sound-evoked suprathreshold ABR waves at the level of the auditory nerve (wave I) and inferior colliculus (IC) (wave IV), indicating that BDNF in lower brain regions but not in the auditory cortex improves sound sensitivity during hearing onset. Extracellular recording of IC neurons of BDNF (Pax2) mutant mice revealed that the reduced sensitivity of auditory fibers in these mice went hand in hand with elevated thresholds, reduced dynamic range, prolonged latency, and increased inhibitory strength in IC neurons. Reduced parvalbumin-positive contacts were found in the ascending auditory circuit, including the auditory cortex and hippocampus of BDNF (Pax2) -KO, but not of BDNF (TrkC) -KO mice. Also, BDNF (Pax2) -WT but not BDNF (Pax2) -KO mice did lose basal inhibitory strength in IC neurons after acoustic trauma. These findings suggest that BDNF in the lower parts of the auditory system drives auditory fidelity along the entire ascending pathway up to the cortex by increasing inhibitory strength in behaviorally relevant frequency regions. Fidelity and inhibitory strength can be lost following auditory nerve injury leading to diminished sensory outcome and increased central noise.
- Klíčová slova
- BDNF, Central hyperactivity, High-spontaneous rate, low-threshold fibers, Homeostatic plasticity, Inferior colliculus, Sound detection threshold,
- MeSH
- colliculus inferior patologie patofyziologie MeSH
- delece genu MeSH
- hluk * MeSH
- integrasy metabolismus MeSH
- kochlea metabolismus MeSH
- mozkový neurotrofický faktor metabolismus MeSH
- myši knockoutované MeSH
- promotorové oblasti (genetika) genetika MeSH
- receptor trkC metabolismus MeSH
- rizikové faktory MeSH
- sluch MeSH
- sluchové kmenové evokované potenciály MeSH
- sluchové korové centrum metabolismus patologie patofyziologie MeSH
- sluchový práh MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- Cre recombinase MeSH Prohlížeč
- integrasy MeSH
- mozkový neurotrofický faktor MeSH
- receptor trkC MeSH
The two inferior colliculi (IC) are paired structures in the midbrain that are connected to each other by a bundle of commissural fibers. The fibers play an important role in coordinating sound signal processing between the two inferior colliculi. This study examined inter-collicular suppression on sound signal processing in amplitude domain of mice by measuring the rate-amplitude functions (RAFs) of neurons in one IC during the electrical stimulation of the opposite IC. Three types (monotonic, saturated and non-monotonic) RAFs of collicular neurons were measured before and during inter-collicular suppression. Inter-collicular suppression significantly increased the slope, decreased the dynamic range and narrowed down the responsive amplitude of all RAFs to high amplitude level but did not change the type of most (36/43, 84 %) RAFs. As a result, all types of RAFs were compressed at a greater degree at low than at high sound amplitude during inter-collicular suppression. These data indicate that inter-collicular suppression improve sound processing in the high amplitude domain.
- MeSH
- colliculus inferior fyziologie MeSH
- elektrická stimulace MeSH
- myši MeSH
- neurony fyziologie MeSH
- sluchová percepce fyziologie MeSH
- zvířata MeSH
- Check Tag
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
There are powerful pathways descending from the auditory cortex (AC) to the inferior colliculus (IC), yet their function is not fully understood. The aim of this study is to examine the effects of a reversible cortical inactivation, achieved by cooling of the AC, on the responses of neurons in the rat IC. Extracellular single-unit or multi-unit activity was recorded in the IC of anaesthetized rats with a 16-channel multielectrode probe introduced along the IC dorso-ventral axis through the dorsal cortex (DCIC) to the central nucleus of the IC (CIC). Cooling of the AC produced an increase in spontaneous activity and magnitude of the sound-evoked response in 47% of the IC neurons. Maximal changes in the neuronal activity were observed in the DCIC and the central part of the CIC. The final segments of the sustained responses to 60 ms stimuli and the off responses were more affected than the onset segments. Inactivation of the AC resulted in a suppression of the post-excitatory inhibition and neuronal adaptation, which was reflected in a pronounced enhancement of synchronized responses to a series of fast repeated clicks. The response parameters recovered, at least partly, to the pre-cooling levels 1 h after the cooling cessation. The frequency tuning properties of the IC neurons did not show any significant changes during the cooling period. The results demonstrate that AC cooling inactivates excitatory corticofugal pathways and results in a less activated intrinsic inhibitory network in the IC.
- Klíčová slova
- Auditory cortex, Cooling, Cortical inactivation, Efferent system, Inferior colliculus, Neurons,
- MeSH
- akustická stimulace MeSH
- časové faktory MeSH
- colliculus inferior metabolismus patologie patofyziologie MeSH
- fyziologická adaptace MeSH
- GABAergní neurony metabolismus MeSH
- nervový útlum MeSH
- potkani Long-Evans MeSH
- sluchová dráha patofyziologie MeSH
- sluchové evokované potenciály MeSH
- sluchové korové centrum metabolismus patologie patofyziologie MeSH
- terapeutická hypotermie * MeSH
- termoregulace * MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- srovnávací studie MeSH
In previous studies (Grécová et al., Eur J Neurosci 29:1921-1930, 2009; Bures et al., Eur J Neurosci 32:155-164, 2010), we demonstrated that after an early postnatal short noise exposure (8 min 125 dB, day 14) changes in the frequency tuning curves as well as changes in the coding of sound intensity are present in the inferior colliculus (IC) of adult rats. In this study, we analyze on the basis of the Golgi-Cox method the morphology of neurons in the IC, the medial geniculate body (MGB) and the auditory cortex (AC) of 3-month-old Long-Evans rats exposed to identical noise at postnatal day 14 and compare the results to littermate controls. In rats exposed to noise as pups, the mean total length of the neuronal tree was found to be larger in the external cortex and the central nucleus of the IC and in the ventral division of the MGB. In addition, the numerical density of dendritic spines was decreased on the branches of neurons in the ventral division of the MGB in noise-exposed animals. In the AC, the mean total length of the apical dendritic segments of pyramidal neurons was significantly shorter in noise-exposed rats, however, only slight differences with respect to controls were observed in the length of basal dendrites of pyramidal cells as well as in the neuronal trees of AC non-pyramidal neurons. The numerical density of dendritic spines on the branches of pyramidal AC neurons was lower in exposed rats than in controls. These findings demonstrate that early postnatal short noise exposure can induce permanent changes in the development of neurons in the central auditory system, which apparently represent morphological correlates of functional plasticity.
- Klíčová slova
- Central auditory system, Critical period, Dendrites, Noise exposure, Rat, Spines,
- MeSH
- akustická stimulace MeSH
- colliculus inferior růst a vývoj patologie MeSH
- dendritické trny patologie MeSH
- hluk škodlivé účinky MeSH
- metathalamus růst a vývoj patologie MeSH
- nervová síť patologie MeSH
- neurony patologie MeSH
- neuroplasticita MeSH
- novorozená zvířata MeSH
- potkani Long-Evans MeSH
- pyramidové buňky patologie MeSH
- sluchová dráha patologie MeSH
- sluchové korové centrum růst a vývoj patologie MeSH
- věkové faktory MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH