Intracellular Response Properties of Units in the Dorsal Cochlear Nucleus of Unanesthetized Decerebrate Gerbil

Abstract

Intracellular recording experiments on the dorsal cochlear nuclei of unanesthetized decerebrate gerbils were conducted. Acceptable recordings were those in which resting potentials were -50 mV or less and action potentials (APs) were > or = 40 mV. Responses to short-duration tones and noise, and to current pulses delivered via recording electrodes, were acquired. Units were classified according to the response map scheme (types I-IV). Ninety-two acceptable recordings were made. Most units had simple APs (simple-spiking units); nine units had both simple and complex APs, which are bursts of spikes embedded on slow, transient depolarizations (complex-spiking units). Of 83 simple-spiking units, 46 were classified as follows: type I/III (9 units), type II (9 units), type III (25 units), type IV (2 units), and type IV-T (1 unit). One complex-spiking unit was classifiable (a type III unit); six were unclassifiable because of weak acoustic responses. Classifying 39 other simple-spiking units and 2 complex-spiking units was impossible, because they were either injured or lost before sufficient data were acquired. Many simple-spiking units showed depolarization or hyperpolarization (approximately 5-10 mV) during acoustic stimulation; some were hyperpolarized during the stimulus-off period. Type I/III units were not hyperpolarized during off-best-frequency (off-BF) stimulation. In contrast, many type II units were hyperpolarized by off-BF frequencies, suggesting that they received strong inhibitory sideband inputs. When inhibited, some type III units were hyperpolarized. Type IV units were hyperpolarized during inhibition even at low levels (<60 dB SPL); sustained depolarizations occurred only at higher levels, suggesting that they receive strong inhibitory and weak excitatory inputs. Several intracellular response properties were statistically different from those of extracellularly recorded units. Intracellularly recorded type II units had higher thresholds and lower maximum BF-driven and noise-driven rates than their extracellularly recorded counterparts. Type I/III units recorded intracellularly had lower maximum BF-driven rates. Type III units recorded intracellularly had higher maximum noise rates compared with those recorded extracellularly. Weaker acoustic responses most likely result from membrane disruption, but heightened responses may be related to weakened chloride-channel-dependent inhibition due to altered driving forces resulting from KCl leakage. Firing rates of simple-spiking units increased monotonically with increasing levels of depolarizing current pulses. In contrast, many complex-spiking units responded nonmonotonically to depolarizing current injection. The monotonic rate-versus-current curves and the nonmonotonic rate-versus-sound level curves of type IV and III units suggest that the acoustic behavior is the result of extrinsic inhibitory inputs and not due solely to intrinsic membrane properties.

Modeling inhibition of type II units in the dorsal cochlear nucleus

“…This was done by setting the spike threshold high enough that the I2-cells could not be brought to threshold by their spontaneously active excitatory (AN) inputs. Intracellular recordings in the decerebrate gerbil indicate that type II units have higher spike thresholds than other unit types in the DCN (Ding and Voigt 1997). These higher thresholds, however, could be the result of either an intrinsic mechanism or spontaneous inhibitory inputs to type II units that tonically hyperpolarize their membranes.…”

“…Spirou and Young (1991), however, were able to use a two-tone stimulus paradigm to demonstrate the existence of sideband inhibition. Ding and Voigt (1997) have recently observed hyperpolarizing responses to off best-frequency tones in intracellularly recorded type II units.…”

Stimulus-timing-dependent modifications of rate-level functions in animals with and without tinnitus

“…The best frequency (BF) of each fusiform cell was assessed based on its receptive field, constructed by counting the number of spikes produced in response to a total of 7,600 sound bursts over a frequency range of 100 -24 kHz (in 0.2-octave steps) and an intensity range of 0 -90 dB (in 5-dB steps). Poststimulus histograms, tone, and noise RLFs were collected to determine the unit type based on previously described criteria (Evans and Nelson 1973;Young and Brownell 1976;Young 1980;Rhode et al 1983;Stabler et al 1996;Ding and Voigt 1997) (see 2 representative examples in Fig. 4, A and B).…”

“…basal dendrites demonstrate monotonic and sigmoid-like RLFs with either low thresholds and saturation plateaus for low to medium sound levels or high thresholds and nonsaturating responses (Sachs and Abbas 1974;Yates et al 1990;Muller et al 1991). In contrast, fusiform cells show more complex RLFs with monotonic and nonmonotonic shapes and various dynamic ranges and saturation levels (Evans and Nelson 1973;Young and Brownell 1976;Young 1980;Rhode et al 1983; Stabler et al 1996;Ding and Voigt 1997). This complexity is assumed to arise mainly from the inhibition provided by both the DCN circuitry via projections of the vertical cells as well as projections of the D-multipolar/stellate cells from the ventral domain of the CN (VCN) onto fusiform cells.…”

Single neuron recordings in dorsal cochlear nucleus (DCN) of awake gerbil

“…Type I/III units in the awake gerbil might turn into type III units in the decerebrate gerbil. There is evidence that some fusiform cells in the decerebrate gerbil had type I/III RMs (n = 2, 15%), but the vast majority were type III units (n = 8, 62%, Ding and Voigt, 1997).…”