Temporal processing from the auditory nerve to the medial nucleus of the trapezoid body in the rat

Abstract

This investigation examines temporal processing through successive sites in the rat auditory pathway: auditory nerve (AN), anteroventral cochlear nucleus (AVCN) and the medial nucleus of the trapezoid body (MNTB). The degree of phase-locking, measured as vector strength, varied with intensity relative to the cell’s threshold, and saturated at a value that depended upon stimulus frequency. A typical pattern showed decline in the saturated vector strength from approximately 0.8 at 400 Hz to about 0.3 at 2000 Hz, with similar profiles in units with a range of characteristic frequencies (480–32 000 Hz). A new expression for temporal dispersion indicates that this variation corresponds to a limiting degree of temporal imprecision, which is relatively consistent between different cells. From AN to AVCN, an increase in vector strength was seen for frequencies below 1000 Hz. At higher frequencies, a decrease in vector strength was observed. From AVCN to MNTB a tendency for temporal coding to be improved below 800 Hz and degraded further above 1500 Hz was seen. This change in temporal processing ability could be attributed to units classified as primary-like with notch (PL_N). PL_N MNTB units showed a similar vector strength distribution to PL_N AVCN units. Our results suggest that AVCN PL_N units, representing globular bushy cells, are specialised for enhancing the temporal code at low frequencies and relaying this information to principal cells of the MNTB.

Introduction

Temporal coding of sound may be manifested by the intervals between neural responses being multiples of the period of the sound wave (Kiang et al., 1965, Rose et al., 1959). The occurrence of action potentials in this manner has been termed phase-locking (Rose et al., 1967). Phase-locking has been investigated extensively in mammals such as the cat (Kiang et al., 1965, Johnson, 1980, Joris et al., 1994a, Joris et al., 1994b), squirrel monkey (Rose et al., 1967, Geisler et al., 1974), chinchilla (Woolf et al., 1981) and guinea-pig (Tasaki, 1954, Harrison and Evans, 1979). However little is known of phase-locking ability of the rat.

Investigations of temporal coding in small mammals, such as the guinea-pig and chinchilla, indicate that phase-locking is detectable up to 3500 Hz (Harrison and Evans, 1979, Woolf et al., 1981, Palmer and Russell, 1986). This phase-locking limit is less than the 5000–6000 Hz limit seen in cats (Rose et al., 1959, Kiang et al., 1965). Palmer and Russell (1986) have shown that a limiting factor for phase-locking ability in guinea-pigs is the hair-cell membrane time constant, although variation in the transmission time (presumably due to synaptic processes) has also been suggested to affect the high-frequency limit of phase-locking (Anderson et al., 1971). In addition, Møller, 1972, Møller, 1976a, Møller, 1976b investigated the temporal responses of auditory nerve (AN) and cochlear nucleus units in rats to amplitude-modulated sounds. These studies indicated that AN fibres have a higher cut-off frequency than cochlear nucleus units for the coding of the amplitude modulation. Møller attributed this degradation in coding to an increase in temporal spread in the cochlear nucleus. The ability to phase-lock may be compromised further as we move up the auditory pathway due to the additive effect of jitter from one stage of processing to the next (Köppl, 1997).

Although variation in transmission time and membrane time constants play a role in limiting phase-locking, other mechanisms also exist to enhance phase-locking, particularly at low frequencies. Recent evidence has shown that bushy cell types in the anteroventral cochlear nucleus (AVCN) of the cat are able to phase-lock in a more precise manner and show higher entrainment capabilities than AN fibres for frequencies below 1000 Hz (Joris et al., 1994a, Joris et al., 1994b). This improved ability to process temporal information may be related to convergence and coincidence detection of AN input to the AVCN (Carney, 1990, Joris et al., 1998). This increase in phase-locking ability is seen in bushy cell types of the AVCN, in particular globular bushy cells (Joris et al., 1994a, Joris et al., 1994b). Globular bushy cells send excitatory input via the trapezoid body to cells in the contralateral medial nucleus of the trapezoid body (MNTB; Banks and Smith, 1992).

Anatomically and physiologically, the principal cells of the MNTB closely resemble the bushy cells of the AVCN (Morest, 1968, Smith et al., 1998). Calyces of Held are present on the soma of both cell types (Cant and Morest, 1979, Lorente de Nò, 1933, Lorente de Nò, 1981, Banks and Smith, 1992, Lenn and Reese, 1966, Smith et al., 1998). In response to tones, AVCN bushy and MNTB principal cells bear the hallmarks of the primary-like (PL) and primary-like with notch (PL_N) unit types (Smith et al., 1998, Wu and Kelly, 1993). Short time constants and highly non-linear current–voltage relationships are also features shared with the bushy cells (Banks and Smith, 1992, Wu and Kelly, 1991, Wu and Kelly, 1993, Manis and Marx, 1991, Paolini et al., 1997, Paolini and Clark, 1998, Oertel, 1999) which enable them to reproduce rapid trains of action potentials.

The similarities of the bushy cells and MNTB principal cells give the impression of a pathway for precise processing of the temporal code. In this investigation we will determine the limiting frequency for temporal coding in the rat assessed in this pathway. A fixed degree of temporal imprecision produces a wide variety of vector strengths, depending on the stimulus frequency. Köppl (1997) introduced ‘temporal dispersion’, a measure of the temporal spread of action potentials. The two critical advantages of using temporal dispersion rather than vector strength are that temporal dispersion can be compared across frequencies, and that the manner in which vector strength varies with frequency may be understood in terms of a fixed or frequency-independent degree of temporal imprecision. In this paper we introduce an improved measure of temporal dispersion.