The present report describes the physiology and anatomy of 17 intracellularly recorded and …

• Abstract
• Introduction
• Methods
• Results
• Discussion
• Miscellaneous
• References
• Table 1
• Table 2
• Figures

The cochlear nuclei are the sole target of the auditory nerve (AN) and as such represents an obligatory processing stage inthe ascending auditory pathway. The laminated dorsal cochlearnucleus (DCN) contains a variety of morphological cell types exhibitingdiverse physiological responses. The outputs of the DCN arisefrom fusiform cells and giant cells, which project via the dorsalacoustic stria to the contralateral inferior colliculus (Adamsand Warr 1976). Fusiform cells are readily identified by largecell bodies and bipolar dendritic fields (Brawer et al. 1974;Lorente de Nó 1981). In the superficial layer, spinous apicaldendrites interact through a network of granule cells and cartwheelcells (Berrebi and Mugnaini 1991; Golding and Oertel 1997; Mugnainiet al. 1980) with somatosensory (Itoh et al. 1987; Weinberg andRustioni 1987; Wright and Ryugo 1996), vestibular (Burian andGstoettner 1988; Kevetter and Perachio 1989), and descending auditoryinputs (Benson and Brown 1990; Weedman and Ryugo 1996). The distalportion of the basal dendrite is excited by the descending branchof the auditory nerve (Smith and Rhode 1985), while the soma andproximal dendrites are likely inhibited by vertical cells (Saint-Marieet al. 1991; Voigt and Young 1980, 1990) and possibly by stellatecells of the posteroventral cochlear nucleus (PVCN) (Oertel etal. 1990; Zhang and Oertel 1994).

There are several theories regarding fusiform cell function. For example, strong sideband inhibition may serve to enhancethe representation of spectral peaks (Rhode and Greenberg 1994)or to extend dynamic range in the presence of noise (Palmer andEvans 1982). DCN neurons better code the envelopes of amplitude-modulatedstimuli than do auditory nerve fibers (Backoff et al. 1999; Kimet al. 1990), leading to the postulation of a "second axis" thatcodes for envelope frequency (Kim et al. 1990) or periodicitypitch (Langner and Schreiner 1996). Finally, recent evidence hasled to the theory that the DCN extracts spectral cues relevantfor sound localization. The head-related transfer function (HRTF)of the cat contains a prominent notch whose center frequency variesbetween 8 and 30 kHz according to the elevation of the sound source(Musicant et al. 1990; Rice et al. 1992). This frequency rangehas an enlarged representation in the cat DCN as compared withthe cochlea (Spirou et al. 1993). Type IV units, an importantsubset of DCN projection neurons, show sensitivity to both thewidth and center frequency of notches in broadband stimuli (Nelkenand Young 1994; Spirou and Young 1991), as do type III units ingerbils (Parsons et al. 2001).

The present report describes the physiology and anatomy of 17 intracellularly recorded and labeled fusiform cells from theDCN of anesthetized gerbils. The fusiform cells in gerbils andcats differ in their physiological response properties in thedecerebrate preparation. In particular, the incidence of typeIV units in the gerbil is less than one-third that reported inthe cat (Davis et al. 1996; Shofner and Young 1985). Antidromicstimulation studies in the cat indicate that at least a portionof the type IV unit population corresponds to fusiform cells (Young1980). Direct intracellular recording and labeling studies, however,suggest that gerbil fusiform cells are not type IV units (Dinget al. 1999). This difference across species in the response propertiesof an important projection neuron motivates one aim of this study:to make a detailed quantitative comparison of gerbil fusiformcell anatomy to that of the cat. Golgi studies in the cat providea suitable database of anatomical measurements for comparison(Blackstad et al. 1984), including the dimensions of each dendriticarbor. The anatomical analysis of this study suggests, in part,that gerbil fusiform cells may be electrotonically more compactthan those of the cat, and that this difference may account forsome of the observed differences in acoustic responseproperties.

Another issue is that fusiform cells exhibit a variety of response properties. In the decerebrate preparation, they have typeIII unit and type IV unit response maps (Ding et al. 1999; Young1980). In anesthetized preparations, fusiform cells exhibit pauser/buildup,chopper, or onset discharge patterns, depending on stimulus conditions(Hancock and Voigt 2002; Rhode et al. 1983; Rhode and Smith 1986;Smith and Rhode 1985). The existence of such variations must berelated to the complexity of the neural circuits with which fusiformcells interact. But are the cell-to-cell differences merely theresult of random "wiring" differences, or do they reflect underlyingprinciples of organization? This question motivates a second aim:to make a quantitative comparison of fusiform cell physiologyand morphology in cats and gerbils. Certain physiological characteristicswere indeed found to have specific anatomical correlates. Spontaneousrate (SR) was related to the disposition of the basal dendrites,input resistance was correlated with apical dendrite total length,and the discharge pattern at best frequency (BF) was correlatedwith fusiform cell orientation. It appears that neighboring fusiformcells may have different physiological properties and hence differentsignal processing capabilities by virtue of cell-to-cell variationsinmorphology.

This work represents part of the doctoral dissertation of K. E. Hancock.