Neural circuits mediating olfactory-driven behavior in fish

Abstract

The fish olfactory system processes odor signals and mediates behaviors that are crucial for survival such as foraging, courtship, and alarm response. Although the upstream olfactory brain areas (olfactory epithelium and olfactory bulb) are well-studied, less is known about their target brain areas and the role they play in generating odor-driven behaviors. Here we review a broad range of literature on the anatomy, physiology, and behavioral output of the olfactory system and its target areas in a wide range of teleost fish. Additionally, we discuss how applying recent technological advancements to the zebrafish (Danio rerio) could help in understanding the function of these target areas. We hope to provide a framework for elucidating the neural circuit computations underlying the odor-driven behaviors in this small, transparent, and genetically amenable vertebrate.

Keywords: anatomy and physiology; behavior; habenula; hypothalamus; olfactory bulb; olfactory epithelium; teleost; zebrafish.

FIGURE 1

Organization of the olfactory bulb network. Odorants are detected in the olfactory epithelium by three types of sensory neurons (microvillous, ciliated, and crypt cells) that project to different glomeruli located in different areas of the olfactory bulb. Ciliated cells mainly project to the dorsal and medial olfactory bulb; microvillous cells project to the lateral olfactory bulb (Sato et al., 2005, 2007). Crypt cells project to a dorsomedial domain in zebrafish and to a ventral domain in carp (Hamdani el and Doving, 2006; Gayoso et al., 2012). In each glomerulus, olfactory sensory neuron axons contact dendrites of mitral cells, the output cells of the olfactory bulb. Inhibitory interneurons called granules cells are located in the deepest layer of the bulb and modulate the activity of mitral cells. Solid lines represent connections described in zebrafish. Dotted lines represent connections described in other fish species. OE: olfactory epithelium, OB: olfactory bulb, ON: olfactory nerve, POFL: primary olfactory fiber layer, GL: glomerular layer, ECL: external cell layer, ICL: internal cell layer.

FIGURE 2

Fish olfactory system. Primary projections from olfactory sensory neurons to the olfactory bulb or telencephalon are depicted in purple. Secondary olfactory projections from the olfactory bulb to the telencephalon and diencephalon are depicted in green. A putative olfacto-motor pathway connecting the posterior tubercle to executive motor centers in the mesencephalon, described in lampreys, is depicted in red. Solid lines represent connections described in zebrafish. Dotted lines represent connections described in other fish species. OE: olfactory epithelium, OB: olfactory bulb, TE: telencephalon, Dp: dorsal-posterior part of the telencephalon, Hb: habenula, Vv: ventral nucleus of the ventral telencephalon, OT: optic tectum, PT: posterior tubercle, HT: hypothalamus, CB: cerebellum, MLR: mesencephalic locomotor region; RST: reticulo-spinal tract, SC: spinal cord.