Spatial representation of frequency in the rat dorsal nucleus of the lateral lemniscus as revealed by acoustically induced c-fos mRNA expression
Introduction
The conventional view, based largely on electrophysiological studies in cats (e.g., Aitkin et al., 1970), is that the dorsal nucleus of the lateral lemniscus (DNLL) is tonotopically organized with a dorsal (low frequency) to ventral (high frequency) representation. This dorsal-to-ventral organization in cats is further supported by the topography of connections between the DNLL and other tonotopically organized auditory structures, such as the anteroventral cochlear nucleus, the lateral and medial superior olivary nuclei, and the inferior colliculus (e.g., Shneiderman et al., 1988Shneiderman et al., 1998). Based on the topography of projections between the DNLL and inferior colliculus, Merchán et al. (1994) and Kelly et al. (1998)have proposed that the DNLL in the rat is organized differently than in the cat, and that the rat DNLL has a concentric, inside-to-outside, tonotopic organization with high frequencies represented along the rind and low frequencies represented in the core of the nucleus. Others have suggested that the rat DNLL has two mirror-image representations with high frequencies represented dorsally and ventrally and low frequencies represented in the middle (Preuß, 1991; Friauf, 1992; Caicedo and Herbert, 1993).
In a previous study, we reported that the rat DNLL had a dorsal-to-ventral tonotopic organization, but that the organization was crude, when compared to other auditory nuclei, and there was much overlap in the representations of widely divergent frequencies (Saint Marie et al., 1999). In the present study, we have re-examined the tonotopy of the rat DNLL bearing in mind its possible concentric organization. As in our previous studies (Saint Marie et al., 1999; Luo et al., 1999), we have used c-fos mRNA expression to map acoustically driven neural activity. C-fos is an inducible transcription regulatory factor which is expressed in many kinds of neurons throughout the central nervous system in response to sustained physiological levels of stimulation (Morgan and Curran, 1989, Morgan and Curran, 1991). Expression of c-fos mRNA or its product, the Fos protein, has become widely accepted means for mapping neuronal activity in the central nervous system (Sagar and Sharp, 1993). Our results suggest that the frequency representation of the rat DNLL is different from that in the cat in that the rat DNLL has both concentric and dorsal-to-ventral components.
Section snippets
Materials and methods
Material used for the present analysis was produced as part of a previous study in which acoustically induced c-fos mRNA expression was used to describe the tonotopic organization of rat auditory brainstem nuclei (Saint Marie et al., 1999). Fifteen of those cases were used in the present analysis. Each of these cases was exposed to one hour of free-field acoustic stimulation at 80 dB SPL. The stimulus consisted of either pure tones of 2, 8, or 32 kHz or half-octave noise bands centered on 2, 8,
Results
Acoustic stimulation produced robust expression of c-fos mRNA in rat DNLL neurons, especially after high-frequency stimulation (Fig. 1). In cases that were quiet-conditioned and not stimulated acoustically, we found no c-fos expression in the DNLL or elsewhere in the auditory brainstem (Saint Marie et al., 1999). The fewest neurons per case were labeled after low-frequency stimulation with 2-kHz tones or half-octave noise bands centered on 2 kHz (Table 1). Three times as many neurons per case
Discussion
In a previous study we demonstrated that acoustical stimulation with either 2-, 8-, or 32-kHz sounds at 80 dB SPL produced distinct, largely non-overlapping bands of c-fos labeling in the anteroventral, posteroventral and dorsal cochlear nuclei, the medial nucleus of the trapezoid body, the lateral superior olive, and the inferior colliculus (Saint Marie et al., 1999). Some tonotopy was also noted in the DNLL, but that was described as crude with much overlap in the representation of widely
Acknowledgements
The authors thank Robbin Newlin and David A. Stanforth for valuable technical assistance. Grant sponsors: The House Ear Institute (R.L.S.M., L.L.), The National Institute on Deafness and Other Communication Disorders (NIH) (grant numbers: PHS RO1 DC-00726 (R.L.S.M.) and PHS RO1 DC-00139 (A.F.R.)) and The Research Service of the VA (A.F.R.).
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Present address: R.W. Johnson Pharmaceutical Research Institute, 3535 General Atomic Court, San Diego, CA 92121, USA.