Adaptation in auditory-nerve fibers: A revised model

Abstract

Adaptation of firing rates in auditory-nerve fibers appears to reflect two distinct processes. Rapid adaptation occupies the first few milliseconds of response and is superimposed upon short-term adaptation which has a time constant of about 40 ms. The properties of the two processes are reviewed and compared, and a phenomenological model is developed that successfully accounts for them. The model consists of several stages which have been tentatively associated with underlying physiological processes. In the first stage stimulus intensity is transformed by a static nonlinearity, followed by a low-pass filter. The filtered output may correspond to the hair-cell receptor potential. It modulates the release of a substance that possibly represents synaptic transmitter. Adaptation is produced by the depletion of transmitter which is located in three stores in cascade. A global store with fixed concentration controls the steady-state response and replenishes a local store which is responsible for short-term adaptation. The local store replenishes a rapidly depleted immediate store. Flow between stores is proportional to concentration gradients with the following exceptions. The immediate store is subdivided into independent volumes or sites and there is no flow among sites or back to the local store. A given site becomes activated only when the receptor potential exceeds its particular activation value and the number of activated sites is proportional to the receptor potential. The flow of transmitter from the immediate store is assumed to be proportional to neural firing rate, with some minor modifications described in the text. The properties of the model are determined from the underlying equations and from a computer simulation. The model produces realistic response properties including PST histograms, onset and steady-state rate-intensity functions, incremental and decremental responses, response modulation for amplitude modulated stimuli, and period histograms for low-frequency tones.

A phenomenological model of the synapse between the inner hair cell and auditory nerve: Long-term adaptation with power-law dynamics

“…Although the mechanism that gives rise to synaptic adaptation is not completely understood, it could be caused either by the depletion of neurotransmitter from a readily releasable presynaptic pool of neurotransmitter ͑Moser and Beutner, 2000; Schnee et al, 2005;Goutman and Glowatzki, 2007͒ or by the desensitization of post-synaptic receptors ͑Raman et al, 1994͒. Modeling the adaptation in the IHC-AN synapse has been a focus of extensive research over the last several decades. Early attempts employed a single-reservoir system with loss and replenishment of transmitter quanta ͑Schroeder and Hall, 1974;Sujaku, 1974, 1975͒, and later models added extra reservoirs ͑or sites͒ or more complex principles of transmitter flow control ͑Furukawa and Matsuura, 1978;Furukawa et al, 1982;Ross, 1982Ross, , 1996Schwid and Geisler, 1982;Smith and Brachman, 1982;Cooke, 1986;Meddis, 1986Meddis, , 1988Westerman and Smith, 1988͒. In general, the transmitter in these models lies in reservoirs or sites close to the presynaptic membrane and diffuses between reservoirs within the cell and out of the cell to the synaptic cleft.…”

“…Although addition of extra reservoirs or sites in the model ͑equivalent to adding more exponential processes͒ tends to address more response properties of the AN ͑e.g., Smith and Brachman, 1982;Payton, 1988͒, such a model becomes mathematically intractable, and thus finding a set of parameters that works well for a large set of AN response properties is difficult, if not impossible.…”

Tonotopic Distribution of Short-Term Adaptation Properties in the Cochlear Nerve of Normal and Acoustically Overexposed Chicks

“…This adaptation to a steady-state level occurs in stages, which in the literature are grouped into four classes based on the time constant (t): rapid (t õ 1-10 ms), short-term (t õ 10-100 ms), long-term (t õ 1-10 s), and very long-term (t õ 10-240 s) (Harris and Dallos 1979;Westerman and Smith 1984;Javel 1996). Adaptation models have invoked a series of depletable vesicle Breservoirs^in hair cells to account for the stages (Schwid and Geisler 1982;Smith and Brachman 1982;Geisler and Greenberg 1986;Westerman and Smith 1988). This depletion hypothesis is supported by work on goldfish saccular afferents where excitatory postsynaptic potentials (EPSPs) decrease in amplitude during a constant acoustic stimulus .…”

Computational auditory scene analysis: A representational approach

“…Simple models of adaptation employ a single reservoir of neurotransmitter (Schroeder and Hall [240], Oono and Sujaku [195]), but these are unable to reproduce several important aspects of the physiological data. More recent models (Smith and Brachman [256], Schwid and Geisler [241]) employ multiple reservoirs, and give better agreement with experimental findings at the cost (in general) of increased computational expense.…”