Afferent influences on brain stem auditory nuclei of the chicken: presynaptic action potentials regulate protein synthesis in nucleus magnocellularis neurons

Abstract

_Studies of the avian auditory sytem indicate that neurons in nucleus magnocellularis (NM) and nucleus laminaris of young animals are dramatically altered by changes in the auditory receptor. We examined the role of presynaptic activity on these transneuronal regulatory events. TTX was used to block action potentials in the auditory nerve. TTX injections into the perilymph reliably blocked all neuronal activity in the cochlear nerve and NM. Far-field recordings of sound-evoked potentials revealed that responses returned within 6-12 hr after a single TTX injection. Changes in protein synthesis by NM neurons were measured by determining the incorporation of 3H-leucine using autoradiography.NM neurons on the side of the brain ipsilateral to the TTX injection were compared to normally active cells on the other side of the same tissue section.Grain counts over individual neurons revealed that a single injection of TTX produced a 40% decrease in grain density in ipsilateral NM neurons within 1.5 hr after the TTX injection. However, by 24 hr after a single TTX injection, grain densities were not different on the 2 sides of the brain. Continuous activity blockade for 6 hr caused the cessation of amino acid incorporation in a portion of NM neurons and a 15-20% decrease in the remaining neurons. These changes in amino acid incorporation are comparable to those following complete removal of the cochlea (Steward and Rubel, 1965). We also examined NM for neuron loss and soma shrinkage after blocking eighth nerve action potentials.TTX injected every 12 hr for 46 hr caused a 20% neuron loss and an 6% shrinkage of the remaining neurons. Similar reductions were found following cochlea removal (Born and Rubel, 1965). It is concluded that neuronal activity plays a major role in the maintenance of normal NM neurons. Furthermore, these results

Plasticity in the Development of Afferent Patterns in the Inferior Colliculus of the Rat after Unilateral Cochlear Ablation

“…Mounting evidence suggests that spontaneous rhythmic discharges similar to those first described in the retina (Galli and Maffei, 1988;Meister et al, 1991;Wong et al, 1993;Feller et al, 1996Feller et al, , 1997 are present at various levels of the developing auditory system before the onset of hearing (Romand and Ehret, 1990;Rübsamen and Schäfer, 1990;Gummer and Mark, 1994;Lippe, 1994Lippe, , 1995Kotak and Sanes, 1995;Kros et al, 1998;Jones and Jones, 2000). Findings in the embryonic chick (Lippe, 1994(Lippe, , 1995 suggest that the synchronous and rhythmic firing observed in the auditory nerve and brainstem is generated peripherally because it is abolished after cochlear removal or injection of tetrodotoxin into the perilymph (Koerber et al, 1966;Born and Rubel, 1988;Born et al, 1991;Lippe, 1994).…”

“…These observations, paired with the present data demonstrating considerable developmental plasticity after unilateral cochlear ablation, suggest that the auditory periphery plays a role in the development of afferent patterns within the IC. Although the rat cochlea is still immature during the first 2 postnatal weeks and compound action potentials recorded at the round window do not appear until between P12 and P13 (Uziel et al, 1981;Rybak et al, 1992), there is rhythmic endogenous activity within the ascending system of various species before hearing onset that is thought to be generated peripherally (Koerber et al, 1966;Born and Rubel, 1988;Romand and Ehret, 1990;Rübsamen and Schäfer, 1990;Born et al, 1991;Gummer and Mark, 1994;Lippe, 1994Lippe, , 1995Kotak and Sanes, 1995;Kros et al, 1998;Jones and Jones, 2000). If such endogenous activity conveys meaningful representations of correlated, peripheral events to the IC, then the segregation of afferents within the central nucleus into ear-specific sublayers (i.e., formation of afferent bands within sublayers based on laterality) may involve activity-dependent mechanisms.…”

Trophic Support of Cultured Spiral Ganglion Neurons by Depolarization Exceeds and Is Additive with that by Neurotrophins or cAMP and Requires Elevation of [Ca2+]iwithin a Set Range

“…Blockade of afferent input increases death in vivo in central (Catsicas et al, 1992;Galli-Resta et al, 1993) and peripheral neurons (Wright, 1981;Furber et al, 1987;Meriney et al, 1987;Maderdrut et al, 1988). In the avian auditory system, removal of the cochlea causes rapid atrophic changes, culminating in a 25-30% loss of neurons in the target, nucleus magnocellularis (Born and Rubel, 1985;Steward and Rubel, 1985;Sie and Rubel, 1992); blockade of electrical activity results in rapid atrophic changes and loss of magnocellularis neurons comparable with those after complete cochlear ablation (Born and Rubel, 1988;Pasic and Rubel, 1989;Rubel et al, 1990;Sie and Rubel, 1992).…”

Deafness Disrupts Chloride Transporter Function and Inhibitory Synaptic Transmission

“…Many anatomical studies have shown that reduced neural activity or deafferentation lead to postsynaptic cell death, atrophy, and altered metabolism in the central auditory nervous system (LeviMontalcini, 1949;Webster and Webster, 1979;Parks, 1981;Deitch and Rubel, 1984;Durham and Rubel, 1985;Born and Rubel, 1988;McMullen et al, 1988;Hashisaki and Rubel, 1989;Hyson and Rubel, 1989). However, in vivo electrophysiology studies show that the remaining synapses do function and may undergo physiological alterations.…”