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Connectional Basis for Frequency Representation in the Nuclei of the Lateral Lemniscus of the Bat Eptesicus Fuscus

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Connectional Basis for Frequency Representation in the Nuclei of the Lateral Lemniscus of the Bat Eptesicus Fuscus The Journal of Neuroscience October 1966, 6(10): 2926-2940 Connectional Basis for Frequency Representation in the Nuclei of the Lateral Lemniscus of the Bat Eptesicus fuscus E. Covey* and J. H. Casseday*l”f Departments of *Surgery (Otolaryngology) and *s-j-Psychology, Duke University, Durham, North Carolina 27710 To study the role of the lateral lemniscus as a link in the as- these cytoarchitectural distinctions. The intermediate and ven- cending auditory pathway, injections of neuronal tracers were tral nuclei of the lateral lemniscus receive their major input placed in the anteroventral cochlear nucleus (AVCN) and in the from the contralateral cochlear nucleus and project to the ip- inferior colliculus of the bat Eptesicus fuscus. To correlate the silateral inferior colliculus (Zook and Casseday, 1982b, 1985). anatomical results with tonotopic organization, the character- These connections provide a “monaural” pathway to the infe- istic frequency of cells at each injection site was determined rior colliculus in Pteronotus and are more likely involved in electrophysiologically. Pathways from AVCN diverge to 3 ma- frequency or temporal analysis than in binaural analysis (Casse- jor targets in the lateral lemniscus, the intermediate nucleus and day and Covey, 1986; Zook and Casseday, 1985). 2 divisions of the ventral nucleus (VNLL). Projections from these In this report we examine the indirect pathways via the in- 3 nuclei then converge at the inferior colliculus. One cell group termediate and ventral nuclei of the lateral lemniscus of Eptes- is particularly notable for its cytoarchitectural appearance. It is icus fiscus. Because the echolocation cries of Eptesicus and referred to here as the columnar area of VNLL because its cells Pteronotus differ greatly in some respects but are similar in that are organized as a tightly packed matrix of columns and rows. they both contain an FM component, we were curious as to The connections of the columnar area are organized in sheets what similarities or differences might be found in the brain-stem that are precisely related to the tonotopic organization of both auditory structures of these 2 species. In examining the brain AVCN and the inferior colliculus. Sheets of cells in the dorsal stem of Eptesicus a striking similarity was immediately obvious part of the columnar area receive projections from low-frequen- in the organization of the nuclei of the lateral lemniscus in these cy parts of AVCN and project to low-frequency parts of the 2 species of bats. inferior colliculus. These sheets of connections occupy succes- For this reason we decided to examine these structures in sively more ventral locations as the tonotopic focus of the injec- more detail, using a combination of anatomical and physiolog- tion site increases in frequency. The entire range of frequencies ical techniques, and we report here the connectional basis for audible to the bat is systematically represented along the dor- frequency organization in the nuclei of the lateral lemniscus. sal-ventral dimension of the columnar area. Because each col- We conducted 2 types of experiments: (1) anterograde transport umn is only 20-30 cells in height, frequency representation must from the anteroventral cochlear nucleus to the lateral lemniscus, be compressed in this dimension. Within the columnar area and (2) retrograde transport from the inferior colliculus. In both there is an overrepresentation of frequencies between 25 and 50 types of experiments we determined by electrophysiological kHz, which corresponds roughly to the range of the FM echo- methods the sound frequency to which cells at the center of the location call in Eptesicus. The connections of the other nuclei injection site responded best. In this way we were able to match of the lateral lemniscus are not as precisely related to the ton- the pattern of labeling in the nuclei of the lateral lemniscus with otopic organization of the system as are those of the columnar the tonotopic organization of the source of the afferent projec- area. tions and the target of the efferent projections. We shall describe evidence to show that the division of the lateral lemniscus that A number of distinct auditory pathways ascend to the inferior has the most orderly cytoarchitectural features, the columnar colliculus. Some of these arise directly from the different divi- area, also has the most precise relationship with the tonotopic sions of the cochlear nucleus, whereas others take an indirect organization of the anteroventral cochlear nucleus and the in- route via synapses in the nuclei of the superior olivary complex ferior colliculus. or nuclei of the lateral lemniscus. Previous reports from this laboratory have shown that in the mustache bat, Pteronotus, the Materials and Methods ventral and intermediate nuclei of the lateral lemniscus are hy- Twenty-sevenadult big brown bats, E. fuscus, obtained from the attics pertrophied and have an elegance of organization not matched of local houses, were used in this study. Wheat germ agglutinin con- in the lateral lemniscus of other mammals. The intermediate jugatedto HRP (WGA-HRP) wasinjected in the anteroventralcochlear nucleus is more highly differentiated than it is in the cat (see nucleus (AVCN) of 7 bats, and WGA-HRP or HRP was injected in the Glendenning et al., 198 1; Zook and Casseday, 1982a), and the inferior colliculus of 20 bats. The HRP was obtained from Sigma (type ventral nucleus is clearly divided into 2 parts, one of which has VI) and the WGA-HRP from Sigma or from Dr. R. G. Carey, Barrow Neurobiological Institute. a columnar arrangement of its cells and the other of which does The animals were anesthetized for surgery with methoxyfluorane (Me- not. The pattern of afferent and efferent connections matches tofane) and maintained in a lightly anesthetized state during electro- physiological recording and injection of neuronal tracer substances. The inferior colliculus was exposed by removal of a small portion of the Received Dec. 17, 1985; revised Apr. 14, 1986; accepted Apr. 17, 1986. overlying skull; to expose the cochlear nucleus it was necessary to re- I This work was supported by NIH Grant NS 2 1748 and NSF Grant BNS 82- move part of the lateral lobe of the cerebellum.The bat’s headwas 17357. We thank Cindy Biles for technical assistance. immobilized by clamping its upper jaw in a bite bar. Correspondence should be addressed to Dr. E. Covey, Department of Surgery, To determine the tonotopic organization in and around the injection Box 3943, Duke University Medical Center, Durham, NC 27710. site, we recorded the response of single neurons or multiunit clusters to Copyright 0 1986 Society for Neuroscience 0270-6474/86/102926-15$02.00/O pure-tone stimuli. The stimuli were tone pulses, 10 msec in duration, The Journal of Neuroscience Connections of Lateral Lemniscus in the Bat INLL so Figure2. Photomicrograph of the columnar area and adjacent regions in a frontal section through the left lateral lemniscus. Tissue embedded in celloidin, 20 Mm sections, cresylecht violet stain. mapped with the aid of a camera lucida. The injection sites were re- constructed in the horizontal plane. To show the anterior-posterior extent of anterograde or retrograde transport in the columnar area, we Figure I. Camera lucida drawing showing the cytoarchitecture of the reconstructed the position of the label in a plane orthogonal to the nuclei of the lateral lemniscus in Eptesicus.Columnar area (Vc) is easily columns of cells. identified by its small and densely packed cells and by the beaded or columnar arrangement of the cells along the length of the ascending Results fibers. Drawn in the frontal plane from a 40 pm frozen section stained with cresyl violet. Calibration bar, 100 pm. Cytoarchifecture of the lateral lemniscus The cell groups of the lateral lemniscusin Eptesicusare shown in Figures 1 and 2. The most highly differentiated cell groups with a 1 msec rise-fall time. The tone pulses were presented in a free field, using Polaroid transducers. are the 2 most ventral ones, which we refer to collectively as In all cases neural activity was recorded with the electrode used to the ventral nucleus (WILL). Of these, the columnar division inject HRP or WGA-HRP. In some cases we used electrodes filled with has the most distinct cytoarchitectural features; therefore, its NaCl or KC1 to map the tonotopic organization adjacent to the site at borders can be defined very precisely. After correction for which we later injected the neural tracer. The electrode was advanced shrinkage in processedsections, this wedge-shapedregion mea- with a hydraulic microdrive. Whenever a single unit was encountered, suresapproximately 300 pm dorsoventrally, 600 pm mediola- we determined its characteristic frequency (CF) by manually controlling terally, and 700 pm rostrocaudally. It is composedalmost ex- the oscillator and attenuator and observing the neural response on the clusively of a single cell type: a small darkly staining multipolar oscilloscope and loudspeaker. Otherwise we examined the response to cell about 10 pm in diameter, with round or oval soma, little tones at steps of 50 pm and were usually able to determine best frequency at every step by tuning the combined response of several cells. cytoplasm and an eccentrically located nucleus. Cells of this For injections, micropipettes with tip diameters of l-10 pm were type are tightly packed together in columns parallel to the fibers filled with a 10% solution of HRP or a 5% solution of WGA-HRP in of the lateral lemniscus. Just ventral to the columnar division 0.85% saline. Upon reaching an area containing units with the desired is an areawe refer to asthe multipolar cell area: most of its cells CF, the tracer was injected electrophoretically by applying pulses of have an irregularly shaped soma with multiple large dendrites. positive current (0.5-2.0 pA),7 set on and 7 set off, for periods ranging There are also a few globular and elongate cells in this division.
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