Physiology of electrosensory lateral line lobe neurons in Gnathonemus petersii

In mormyrid electric fish, sensory signals from electroreceptors are relayed to secondary sensory neurons in a cerebellum-like structure known as the electrosensory lateral line lobe (ELL). Efferent neurons and interneurons of the ELL also receive inputs of central origin, including electric organ corollary discharge signals, via parallel fibers and via fibers from the juxtalobar nucleus. To understand the cellular mechanisms of the integration of sensory inputs and central inputs in the ELL, the intracellular activity and ionic properties of the efferent projection neurons and interneurons were examined in an in vitro slice preparation.

We focus here on the electrophysiological properties of the efferent neurons of the ELL network, the large fusiform cells and large ganglion cells, and on a class of γ-aminobutyric acid (GABA)-ergic interneurons known as medium ganglion (MG) cells. In response to current injection through a recording pipette, both types of efferent neuron fire a large narrow spike followed by a large hyperpolarizing afterpotential. The MG cells fire a complex spike which consists of small narrow spikes and a large broad spike. Although the forms of the action potentials in efferent neurons and in MG cells are different, all spikes are mediated by tetrodotoxin (TTX)-sensitive Na⁺ conductances and spike repolarization is mediated by tetraethylammonium (TEA⁺)-sensitive K⁺ conductances. In the presence of TEA⁺, substitution of Ba²⁺ for Ca²⁺ in the bath revealed the presence of a high-voltage-activated Ca²⁺ conductance.

Stimulation of parallel fibers conveying descending input to the ELL molecular layer in vitro evokes an excitatory postsynaptic potential (EPSP), generally followed by an inhibitory postsynaptic potential (IPSP), in the efferent neurons. In MG cells, the same stimulation evokes an EPSP, often followed by a small IPSP. Synaptic transmission at parallel fiber synapses is glutamatergic and is mediated via both N-methyl-D-aspartate (NMDA)- and (AMPA)-type glutamate receptors. The inhibitory component of the parallel fiber response is GABAergic. It is probably mediated via the stellate neurons and the MG cells, which are themselves GABAergic interneurons intrinsic to the ELL network.

A hypothetical neural circuit of the intrinsic connections of the ELL, based on the known morphology of projection neurons and medium ganglion interneurons, is presented. This circuit includes an excitatory and an inhibitory submodule. The excitatory submodule is centered on a large fusiform cell and appears to relay the sensory input as a positive ‘ON’ image of an object. The inhibitory submodule is centered on a large ganglion cell and relays a negative ‘OFF’ image to the next higher level. We suggest that MG cells exert an inhibitory bias on efferent neuron types and that the ELL network output is modulated by the dynamically plastic integration of central descending signals with sensory input.