The electrosensory system of the weakly electric fish Apteronotus leptorhychus
A primer on electrosensory fish
Introduction
The weakly electric fish is one of the few animals capable of electrosensory perception. It emits an electric organ discharge (EOD) from an electric organ located at the tip of its tail, which produces an electric field around its body. This field is distorted by objects in the fish proximity that have conductivities different from the water. Thus, the signals returning to the fish carry information about objects in its surroundings. The fish senses these distorted electrical fields by means of electroreceptors located on its body surface, and uses them for electrolocation.
Figure 1: Principles of Electroreception
The electrosensory lateral line lobe (ELL): The electrosensory system of the weakly electric fish Apteronotus leptorhyncus is one of the most thoroughly analyzed vertebrate sensory systems. The input to this system is derived from the constant frequency discharge (EOD) of the fishes own electric organ at frequencies of 500-1000 Hz. Two types of cutaneous electroreceptor are found; the ampulary receptors are tuned to the low frequency (<20 Hz) fields that arise from biological origins and the tuberous receptors are tuned to the high frequency fields that are generated by the fishes own EOD. These tuberous receptors provide information for electrolocation by measurement of alterations in the amplitude of the EOD that are caused by interference from local objects close to the fish. Tuberous receptors also provide an electrocommunication function through the detection of high frequency "chirps". The electroreceptors are spread over the surface of the fish body and project to four adjacent segments of the ELL where they generate four parallel topographic maps of the fish skin. The most medial of these is innervated by ampulary receptors only. The tuberous receptors trifurcate and project to three parallel maps in the centromedial, centrolateral and lateral (CMS, CLS, LS) segments of the ELL. The initial processing of electrolocation and electrocommunication occurs in these three segments, with the CMS-CLS-LS maps tuned for progressively higher frequencies.
Figure 2: Overview of Electrosensory Pathways
Although signal processing in the three different segments varies in a frequency dependent way, the basic cellular elements that make up the neural networks are similar in each segment. This basic design is illustrated in the figure. A brief description of this circuit follows: Primary afferent input to the ELL arrives from two classes of tuberous type electroreceptor, T-type and P-type. The T-type receptor fires in phase with the EOD cycle, and thus encodes information on the frequency of the perceived EOD. Inputs from T-type receptor have electrical synapses on a unique cell called a spherical cell, which then relays this signal in phase to higher centers in the CNS. The neural circuits that subserve electrolocation receive input from the P-type electroreceptors which encode the strength of the EOD at the skin surface by alterations in the rate of firing. This rate code is processed by two classes of ELL pyramidal cells, the basilar (BP) and non-basilar (NBP) types shown in the figure. The primary input to the BP cell is through glutaminergic synapses on the basilar dendrite. The primary input to the NBP cell is received initially by the type 2 granule cell (G2) through a glutaminergic synapse. The G2 cell then relays an inhibitory GABA signal to the NBP as shown in the figure below. In addition to this simplified scheme, there are additional interneurons which modulate both BP and NBP cells in this circuit, but they are not included here for the sake of clarity.
Figure 3: Neuronal Connections of the Electrosensory Lateral Line Lobe
Feedback regulation of both the BP and NBP cells is mediated by inputs to their apical dendrites. These inputs are of two types; (i) proprioceptive and electroreceptive inputs from a specialized cerebellar structure called the posterior eminetia granularis (EGp) which synapse on the distal regions of the apical dendrites and (ii) electrosensory feedback inputs from the nucleus praeemintialis which synapse at the more proximal regions of the apical dendrites. Both of these feedback inputs use glutaminergic synapses which include major NMDA components. Anatomically, the location of the three functional classes of glutamate synapse (primary afferent, proprioceptive feedback and electrosensory feedback) are separated into three distinct laminae in the ELL. This clear functional and anatomical relationship greatly facilitates the localization of specific molecular elements to the different synapse types.
Further reading: A series of excellent reviews on the biology of electrosensation are available in a recent compendium published by the Journal of Experimental Biology edited by RW Turner, L Maler and M Burrows. J. Exp. Biol. 202 (10), pp 1167-1458, 1999
