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Oscillatory Discharge Across Electrosensory Maps 1257 Changes in EOD Amplitude The Journal of Experimental Biology 202, 1255–1265 (1999) 1255 Printed in Great Britain © The Company of Biologists Limited 1999 JEB2096 OSCILLATORY AND BURST DISCHARGE IN THE APTERONOTID ELECTROSENSORY LATERAL LINE LOBE RAY W. TURNER1,* AND LEONARD MALER2 1Neuroscience Research Group, Department of Cell Biology and Anatomy, University of Calgary, Calgary, Alberta, Canada T2N 4N1 and 2Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Ontario, Canada K1H 8M5 *e-mail: [email protected] Accepted 2 March; published on WWW 21 April 1999 Summary Oscillatory and burst discharge is recognized as a key pyramidal cell frequency tuning in vivo. One is a slow element of signal processing from the level of receptor to oscillation of spike discharge arising from local circuit cortical output cells in most sensory systems. The relevance interactions that exhibits marked changes in several of this activity for electrosensory processing has become properties across the sensory maps. The second is a fast, increasingly apparent for cells in the electrosensory lateral intrinsic form of burst discharge that incorporates a newly line lobe (ELL) of gymnotiform weakly electric fish. Burst recognized interaction between somatic and dendritic discharge by ELL pyramidal cells can be recorded in vivo membranes. These findings suggest that a differential and has been directly associated with feature extraction of regulation of oscillatory discharge properties across electrosensory input. In vivo recordings have also shown sensory maps may underlie frequency tuning in the ELL that pyramidal cells are differentially tuned to the and influence feature extraction in vivo. frequency of amplitude modulations across three ELL topographic maps of electroreceptor distribution. Pyramidal cell recordings in vitro reveal two forms of Key words: oscillatory discharge, dendritic spike, backpropagation, oscillatory discharge with properties consistent with sensory map, apteronotid, electrosensory lateral line lobe. Introduction Oscillatory and burst discharge is recognized as a we will briefly summarize the evidence for oscillatory or burst component of many sensory systems and is now believed to discharge in the ELL gained through in vivo recordings and contribute to feature detection, frequency tuning and focus on recent advances in our understanding of the cellular correlative discharge patterns across wide regions of cortex basis for this activity through in vitro analyses. (Singer, 1993; Singer and Gray, 1995; Laurent et al., 1996; Ritz and Sejnowski, 1997). Oscillatory membrane depolarizations and burst discharge have been detected in Electrosensory lateral line lobe several cell types in the electrosensory system, including The ELL receives direct input from primary afferents electroreceptors, ganglion cells, electrosensory lateral line lobe conveying the activity of ampullary and tuberous receptors. A (ELL) pyramidal and granule cells, and toral giant cells pyramidal cell body layer and granule cell body layer form (Zakon, 1986; Turner et al., 1991b, 1995; Carr and Maler, prominent laminae in the ELL across its medio-lateral extent 1986; Metzner et al., 1998; R. W. Turner and L. Maler, (Fig. 1) (Maler, 1979; Maler et al., 1981, 1991). The ELL is unpublished observations). This activity is generated in further subdivided into four topographic maps or segments of relation to modulations of a weak electric organ discharge electroreceptor distribution that run in a rostro-caudal (EOD) emitted for the purpose of electrolocation or direction: the medial (MS), centromedial (CMS), centrolateral electrocommunication. The electrosensory system is ideal for (CLS) and lateral (LS) segments (Heiligenberg and Dye, 1982; investigating the cellular basis and functional significance of Carr and Maler, 1986). Primary afferent inputs terminate on oscillatory discharge, given the long history of in vivo analysis the basilar dendrite of a basilar pyramidal cell class or on the of electrosensory processing (Bullock and Heiligenberg, 1986; dendrites of a granular cell class I or class II, which are Heiligenberg, 1991; Kramer, 1990, 1996; Moller, 1995; interneurons with cell bodies contained within the granule cell Metzner and Viete 1996a,b; Bell et al., 1999; Metzner, 1999; body layer (Maler et al., 1981). Ascending processes of granule Sugawara et al., 1999; von der Emde, 1999). In this review, cells form excitatory contact with somatic dendrites of a non- 1256 R. W. TURNER AND L. MALER Fig. 1. (A) Cresyl-Violet-stained transverse section of the electrosensory C lateral line lobe (ELL). Dashed lines B indicate the boundaries between four A topographic maps: the medial (MS), centromedial (CMS), centrolateral DML (CLS) and lateral (LS) segments. (B) A m) CMS basilar pyramidal cell in relation µ to the various laminae of the ELL 100 VML (dashed lines). (C) A CMS non-basilar pyramidal cell, illustrating the lack of a tSF 0 basilar dendrite. Note the prominent apical dendritic trees of both basilar and PCL non-basilar pyramidal cells that project -100 Recording distance ( PLX dorsally through the tSF, VML and DML. Cells were labeled with horseradish peroxidase following GCL intrasomatic Biocytin injection. CCb, corpus cerebelli; DML, dorsal DNL molecular layer; DNL, deep neuropil 500 µm 50 µm layer; EGp, eminentia granularis pars posterior; GCL, granule cell layer; PCL, pyramidal cell layer; PLX, plexiform layer; tSF, tractus stratum fibrosum; VML, ventral molecular layer. basilar pyramidal cell class through gap junction contact feature detectors (Gabbiani et al., 1996; Wessel et al., 1996; (Maler 1979; Maler et al., 1981) and inhibitory contacts with Metzner et al., 1998; Gabbiani and Metzner, 1999), setting both basilar and non-basilar pyramidal cells (Maler and global gain control in the ELL via the activation of descending Mugnaini, 1994; see Berman and Maler, 1999). Both basilar feedback inputs (deep basilar pyramidal cells; Bastian and and non-basilar pyramidal cells project apical dendrites Courtright, 1991) and participating in the generation of through an overlying tractus stratum fibrosum (tSF) and negative predictive images to cancel specific sensory inputs subsequently branch several times as they course through the (Bastian, 1995, 1996a,b, 1999). Shumway (1989) was the first ventral molecular layer (VML) and the dorsal molecular layer to demonstrate that pyramidal cells discharge in relation to (DML) (Fig. 1). Although this summary of cell types and ‘map-specific’ behavioral functions in reporting a differential connectivities is very restricted, it reflects our current frequency tuning of amplitude modulations across the CMS, understanding that granule and pyramidal cells are the main CLS and LS maps (see also Metzner et al., 1998). More cell types involved in generating oscillatory discharge in the recently, Metzner and Juranek (1997) carried out selective tuberous electrosensory maps. lesions of ELL maps in vivo and established that cells in the CMS are necessary and sufficient for the final generation of a jamming avoidance response, while LS cells process input In vivo analysis of signal processing in the ELL related to electrocommunicatory ‘chirps’ (see also Metzner, In vivo recordings have identified several behavioral 1999). functions that incorporate ELL pyramidal cell discharge, some Although oscillatory and burst discharge has only recently of which can be localized to specific sensory maps. Cells in the been examined in ELL pyramidal cells in vivo, it is now clear MS respond to ampullary receptors activated by low that ELL pyramidal cells incorporate this activity during frequencies of exogenous electric field modulations (Zakon, electrosensory processing. Some of the first evidence can be 1986; Metzner and Heiligenberg, 1991) and participate in traced to Bastian (1981), who published recordings of a passive electrolocation (i.e. for small invertebrate prey) and rhythmic discharge of pyramidal cells that outlasted a 50 ms electrocommunication (Metzner and Heiligenberg, 1991; step change in EOD amplitude. Saunders and Bastian (1984) Metzner, 1999). Pyramidal cells in the CMS, CLS and LS maps presented some of the first intracellular recordings of spike respond to higher frequencies of EOD modulations conveyed activity per se from pyramidal cells in vivo, which have several by tuberous electroreceptor inputs (Bastian, 1981; Bastian and characteristics in common with the types of oscillatory Courtright, 1991; Saunders and Bastian, 1984; Shumway, discharge recorded in vitro. Similarly, the recordings from ELL 1989; Metzner and Heiligenberg, 1991). The discharge pyramidal cells of Metzner and Heiligenberg (1991) provide properties of pyramidal cells in vivo indicate a role in several indications of burst discharge during the encoding of beat aspects of sensory processing, including the encoding of frequencies in EOD amplitude. Bastian and Courtright (1991) temporal characteristics of field modulations (Bastian, 1981; also reported a higher prevalence of burst output in superficial Saunders and Bastian, 1984; Shumway, 1989), acting as compared with deep basilar pyramidal cells in response to step Oscillatory discharge across electrosensory maps 1257 changes in EOD amplitude. Finally, burst discharges in ELL CMS LS pyramidal cells of Eigenmannia have been analyzed directly A B and shown to have at least a role in the process of feature detection (Gabbiani et al., 1996; Wessel et al., 1996; Metzner et al., 1998; Gabbiani and Metzner, 1999). In vitro analysis
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