The development of some peripheral and central auditory responses in the neonatal cat

doi:10.1016/0006-8993(79)90150-1

Brain Research

Volume 163, Issue 1, 9 March 1979, Pages 49-59

https://doi.org/10.1016/0006-8993(79)90150-1 Get rights and content

Abstract

The development of cochlear nerve action potential thresholds at different frequencies (AP audiograms) and inferior colliculus (IC) single unit thresholds and tuning was examined in barbiturate-anaesthetized kittens. AP thresholds decreased over the whole frequency spectrum during the first 5 weeks of life. Threshold to high-frequency stimulation remained higher in 7-week-old animals than in adults. These results are in contrast to previous reports which have suggested that the AP response and gross cochlear anatomy are mature by the end of the second week. These differences may be due to the fact that the AP audiogram technique provides a measure of the activity of discrete regions along the cochlear partition. IC units in animals younger than 3.5 weeks had significantly elevated thresholds and broader tuning than those of the adult cat. Comparison of AP audiogram and IC unit thresholds in the adult revealed that these indices show similar frequency-dependent sensitivity. The slower maturation revealed by the AP audiogram may be due to the greater number and/or synchrony of cochlear nerve discharges needed to produce the gross AP. If this were the case, perception of suprathreshold sounds might not develop as quickly as thresholds for sound detection.

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During the maturation process, the system develops to process and interpret a broad variety of environmental sounds from simple tones to complex stimuli such as broadband noise and species-specific vocalization. Numerous animal studies have contributed to our understanding about the topographical and functional organization of the auditory pathway (e.g. Merzenich et al., 1975; Whitfield and Evans, 1965) and the development and maturation of auditory functionality (e.g. Moore and Irvine, 1979; Romand, 1987). While pure tone experiments have provided insight into the development of tonotopic organization (e.g. Mrsic-Flogel et al., 2006; Pienkowski and Harrison, 2005) and spectral and temporal response selectivity (Chang et al., 2005) at the cortical level, few developmental studies to date have used complex stimulation to examine the auditory cortex.
Responses to cortical neurons to frequency-modulated (FM) stimuli have been described in various adult animal models. Here, we ask whether FM coding at the cortical level is innate or if it is influenced by postnatal environmental experience. We report on the FM response properties of neurons in core auditory cortex of newborn (P3), 1-month-old (P28) and adult (> 1-year-old) anesthetized chinchillas (Chinchilla laniger). Upward and downward linear FM sweeps spanning frequencies from 0.1 to 20 kHz were presented monaurally at speeds of 0.05 to 0.82 kHz/ms. Results indicated that neurons in neonatal pups were responsive to FM stimulation. While we observed a developmental increase in the selectivity of units for FM sweep direction (p < 0.01, one-way ANOVA), selectivity for sweep speed appeared to be established early in development. Chinchilla pup neurons also demonstrated single-peak (single dominant response during FM sweep presentation) and multi-peak (multiple distinct responses during FM sweep) temporal response patterns to FM stimuli similar to those observed in adults. A developmental increase in the proportion of multi-peak units closely paralleled a previously reported increase in the complexity of pure tone receptive fields. We suggest that units in core auditory cortex of the chinchilla are not uniquely activated by FM sounds but that FM responses are largely predictable based on how changing frequency stimuli interact with the tonal receptive fields of neurons in the auditory cortex.
Unilateral cochlear ablation before hearing onset disrupts the maintenance of dorsal nucleus of the lateral lemniscus projection patterns in the rat inferior colliculus
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During postnatal development, ascending and descending auditory inputs converge to form fibrodendritic layers within the central nucleus of the inferior colliculus (IC). Before the onset of hearing, specific combinations of inputs segregate into bands separated by interband spaces. These bands may define functional zones within the IC. Previous studies in our laboratory have shown that unilateral or bilateral cochlear ablation at postnatal day 2 (P2) disrupts the development of afferent bands from the dorsal nucleus of the lateral lemniscus (DNLL) to the IC. These results suggest that spontaneous activity propagated from the cochlea is required for the segregation of afferent bands within the developing IC. To test if spontaneous activity from the cochlea also may be required to maintain segregated bands of DNLL input, we performed cochlear ablations in rat pups at P9, after DNLL bands already are established. All animals were killed at P12 and glass pins coated with carbocyanine dye, DiI (1,1′-dioctodecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate), subsequently were placed in the commissure of Probst to label the crossed projections from both DNLLs. When compared with surgical controls, experimental results showed a similar pattern of DNLL bands in the IC contralateral to the ablated cochlea, but a disruption of DNLL bands in the IC ipsilateral to the cochlear ablation. The present results suggest that cochlear ablation after DNLL bands have formed may affect the maintenance of banded DNLL projections within the central nucleus of the IC.
Chapter 18 Cochlear implants: cortical plasticity in congenital deprivation
2006, Progress in Brain Research
Citation Excerpt :
These parts of the cortex are not responsive in young animals (Bonham et al., 2004). The finding of increasing bandwidth of units in field A1 contrasts the findings of decreasing bandwidth of tuning curves in the cat inferior colliculus during the first 30–35 days post natal (Moore and Irvine, 1979). Several factors are involved in shaping cortical tuning curves.
Congenital auditory deprivation (deafness) leads to a dysfunctional intrinsic cortical microcircuitry. This chapter reviews these deficits with a particular emphasis on layer-specific activity within the primary auditory cortex. Evidence for a delay in activation of supragranular layers and reduction in activity in infragranular layers is discussed. Such deficits indicate the incompetence of the primary auditory cortex to not only properly process thalamic input and generate output within the infragranular layers, but also incorporate top-down modulations from higher order auditory cortex into the processing within primary auditory cortex. Such deficits are the consequence of a misguided postnatal development. Maturation of primary auditory cortex in deaf animals shows evidence of a developmental delay and further alterations in gross synaptic currents, spread of activation, and morphology of local field potentials recorded at the cortical surface. Additionally, degenerative changes can be observed. When hearing is initiated early in life (e.g., by chronic cochlear-implant stimulation), many of these deficits are counterbalanced. However, plasticity of the auditory cortex decreases with increasing age, so that a sensitive period for plastic adaptation can be demonstrated within the second to sixth months of life in the deaf cat. Potential molecular mechanisms of the existence of sensitive period are discussed. Data from animal research may be compared to electroencephalographic data obtained from cochlear-implanted congenitally deaf children. After cochlear implantation in humans, three phases of plastic adaptation can be observed: a fast one, taking place within the first few weeks after implantation, showing no sensitive period; a slower one, taking place within the first months after implantation (a sensitive period up to 4 years of age); and possibly a third, and the longest one, related to increasing activation of higher order cortical areas.
Modification of tonotopic representation in the auditory system during development
1997, Progress in Neurobiology
During the early development of the bird and the mammalian peripheral auditory system, a restricted range of low-mid frequencies is recorded in immature animals. These early recordings are correlated to the base or mid-basal region of the cochlea which codes high frequencies in the adult. In order to reconcile the functional observations with anatomical ones, two main hypotheses have been put forward: one called the development of the place principle derived from observations of acoustic trauma in chick cochlea and a second derived from auditory nerve fiber recordings in kittens. Whatever the theories, the tonotopic shift during development is a well-established phenomenon in both birds and mammals that could be explained by a synthetic theory including active and passive cochlear processes. The tonotopic shift observed in the central auditory system mimics quite closely the frequency representation of the peripheral auditory system. The same trend is observed in all auditory nuclei including the cortex, except that the frequency representation is more complex because it shows tonotopic maps that can be twisted in three dimensions. From current observations, there is a simultaneous onset of tonotopic maps across auditory nuclei up to the cortex. A hypothesis is presented related to the frequency changes observed in the cochlea that affect the central auditory pathway, along with possible consequences on auditory behavior.
Ontogeny of hearing in the marsupial, Monodelphis domestica, as revealed by brainstem auditory evoked potentials
1995, Hearing Research
Auditory development was studied in the Brazilian short-tailed opossum, Monodelphis domestica, using the brainstem auditory, evoked potential (BAEP). Consistent responses can first be recorded 29 days after birth. The hearing range at the onset of hearing is limited to 5–20 kHz with lowest thresholds of 60 dB SPL at 8–12 kHz. During ontogeny, the hearing range expands towards lower and higher frequencies and thresholds decrease until the adult audiogram is obtained by about day 40. Peak latencies and central conduction times are very long at the onset of hearing and decrease until about day 37.
In Monodelphis, ontogenetic changes of auditory function are in good agreement with those described for eutherian mammals, suggesting that this small marsupial species can be used as a general model system for auditory development in mammals.
Development of tone response thresholds, latencies and tuning in the mouse inferior colliculus
1992, Developmental Brain Research
The development of tone response thresholds, latencies and tuning of neurons in the inferior colliculus (IC) of the mouse has been investigated between postnatal days 10 (first responses) and 20. As in adults, response thresholds of neurons are lowest in the center of the IC compared with other areas right from the beginning of responsiveness at day 10. Thresholds decrease rapidly until at days 16–20 (depending on the characteristics frequency of the neurons) adult levels are reached. Response latencies decrease rapidly to adult levels at days 16–18. Broad frequency tuning curves can be measured at days 10 and 11. From day 12 onwards, tuning curve shapes differentiate and adult diversity occurs which indicates presence of inhibition and summation in the pathway to or within the IC at that early age. The tip lengths of the tuning curves increase faster than the sharpness of the tips (Q_10dBvalues). The developmental courses of the measured parameters are expressed by power functions. The time constants of these functions are used in the discussion of processes underlying the functional maturation in the auditory system of the mouse. The general course of the development of all the here investigated response properties of single neurons in the IC, except tuning curve shape, appears to be determined by maturation at or peripheral to the cochlear level.

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The development of some peripheral and central auditory responses in the neonatal cat

Abstract

Brain Research

Brain Research

Inferior colliculus, II. Development of tuning characteristics and tonotopic organisation in central nucleus of the neonatal cat

J. Neurophysiol.

Inferior colliculus, I. Comparison of response properties of neurons in central, pericentral and external nuclei of adult cat

J. Neurophysiol.

Physiological, behavioral and anatomical correlates of the development of hearing in the mouse

Ann. Otol. (St. Louis)

Glass coated tungsten microelectrodes

Science

The identification of single units in central visual pathways

J. Physiol. (Lond.)

Maturation des re´sponses unitairesa´la stimulation tonale dans le nerf cochle´aire du chaton

J. Physiol. (Paris)

Postnatal development of endocochlear potential and stria vascularis in the cat

Acta oto-laryng. (Stockh.)

Octupos cells in the cochlear nucleus of the cat: heterotypic synapses upon homeotypic neurons

Int. J. Neurosci.

Discharge Patterns of Single Fibres in the Cat's Auditory Nerve

Frequency dependence of tone-burst-generated whole nerve action potentials

J. Acoust. Soc. Amer.