Response Properties of Neurons in the Inferior Colliculus of the Monaurally Deafened Ferret to Acoustic Stimulation of the Intact Ear

Abstract

Response properties of neurons in the central nucleus of the inferior colliculus (ICC) were investigated after unilateral cochlear removal at various ages during infancy. Nineteen ferrets had the right cochlea surgically ablated, either in adulthood or on postnatal day (P) 5, 25, or 40, 3-18 mo before recording. Adult ablations were made on the same day as ("acute," n = 3), or 2-3 mo before ("chronic," n = 3), recording. Two ferrets were left binaurally intact. Single-unit (n = 702) and multiunit (n = 1,819) recordings were made in the ICC of barbiturate-anesthetized ferrets ipsilateral (all ages) or contralateral (P5 and acute adult only) to the intact ear. In binaurally intact animals, tonal stimulation of the contralateral ear evoked excitatory activity at the majority (94%) of recording loci, whereas stimulation of the ipsilateral ear evoked activity at only 33% of recording loci. In acutely ablated animals, the majority of contralateral (90%) and ipsilateral (70%) loci were excited by tonal stimulation of the intact ear. In chronically ablated animals, 80-90% of loci were excited by ipsilateral stimulation. Single-unit thresholds were generally higher for low-best frequency (BF) than for high-BF units, and higher in the ipsilateral than in the contralateral ICC. Analysis of covariance showed highly significant differences between all of the ipsilateral and contralateral groups, but no effects of age at ablation or survival time following ablation, other than that the group ablated at P25 had higher mean ipsilateral thresholds than the groups ablated at P5 or, acutely, in adulthood. Cochlear ablation at P5, 25, or 40 resulted in a significant increase in dynamic ranges of ipsilateral ICC unit rate-intensity functions relative to acutely ablated animals. Dynamic ranges of units in the contralateral ICC of P5-ablated ferrets were also significantly increased compared with those of acutely ablated animals. Cochlear ablation at P5, 25, or 40 resulted in a significant increase in single-unit spontaneous discharge rates in the ICC ipsilateral but not contralateral (P5 only) to the intact ear. These data show that unilateral cochlear removal in adult ferrets leads to a rapid and dramatic increase in the proportion of neurons in the ICC ipsilateral to the intact ear that is excited by acoustic stimulation of that ear. In addition, the data confirm that, in ferrets, cochlear removal in infancy leads to a further increase in responsiveness of individual neurons in the ipsilateral ICC. Finally, the data show that responses in the ICC contralateral to the intact ear are largely but not completely unchanged by unilateral cochlear removal.

Consequences of unilateral hearing loss: Cortical adjustment to unilateral deprivation

“…However, Tucci et al (1999) also measured 2-DG uptake in animals 2 days following ear manipulation, and found the percent difference from SH was on the order of 50 -60%, suggesting that for CHL (and CA) there may be some recovery of activity between 2 days and three weeks. Following unilateral CA, electrophysiological evidence suggests the proportion of units in the opposite IC excited by stimulation of the ipsilateral (intact) ear increases dramatically over time (e.g., McAlpine et al, 1997;Irvine et al, 2003). The mechanism for this change in response characteristics appears to be a rapid reduction in functional inhibition from lemniscal inputs or within the IC itself (e.g., Mossop, et al, 2000;Vale et al, 2004).…”

Rapid Increase in Neural Conduction Time in the Adult Human Auditory Brainstem Following Sudden Unilateral Deafness

“…Evidence from animals with experimentally induced UD indicates that increased neural responsiveness to stimulation of the intact ear occurs over a wide time frame. Initial increases in excitatory responses of cortical and sub-cortical neurons have been demonstrated within minutes to hours post-UD (Popelar et al 1994;Mossop et al 2000), while further changes have been observed a number of months post-UD (McAlpine et al 1997). Therefore, the data from animal studies are consistent with a cascade of multiple processes driving plasticity.…”

“…Experimentally induced UD in adult animals leads to increased neural responsiveness to stimulation of the intact ear (Popelar et al 1994;McAlpine et al 1997;Mossop et al 2000). The changes are greatest in the pathway ipsilateral to the intact ear, probably because this pathway normally receives the strongest input from the deafferented ear (Adams 1979;Coleman and Clerici 1987).…”

“…Functional increases in responsiveness to the intact ear may derive from inactivation of inhibitory pathways that are normally driven by the deafened ear, resulting in 'unmasking' of pre-existing excitatory connections. These changes may involve intracellular signalling pathways that increase or decrease the gain of existing excitatory neurons and synapses (McAlpine et al 1997;Mossop et al 2000;Moore and King 2004). The second mechanism is relatively slow structural changes involving elimination of synapses and expression of new synapses and/ or axons (Moore 1994;McAlpine et al 1997).…”

“…These changes may involve intracellular signalling pathways that increase or decrease the gain of existing excitatory neurons and synapses (McAlpine et al 1997;Mossop et al 2000;Moore and King 2004). The second mechanism is relatively slow structural changes involving elimination of synapses and expression of new synapses and/ or axons (Moore 1994;McAlpine et al 1997). Evidence from animals with experimentally induced UD indicates that increased neural responsiveness to stimulation of the intact ear occurs over a wide time frame.…”