Abstract
High impulse rate in afferent nerves is a common feature in many sensory systems that serve to accommodate a wide dynamic range. However, the first stage of integration should be endowed with specific properties that enable efficient handling of the incoming information. In elasmobranches, the afferent nerve originating from the ampullae of Lorenzini targets specific neurons located at the Dorsal Octavolateral Nucleus (DON), the first stage of integration in the electroreception system. Using intracellular recordings in an isolated brainstem preparation from the shark we analyze the properties of this afferent pathway. We found that stimulating the afferent nerve activates a mixture of excitatory and inhibitory synapses mediated by AMPA-like and GABAA receptors, respectively. The excitatory synapses that are extremely efficient in activating the postsynaptic neurons display unusual voltage dependence, enabling them to operate as a current source. The inhibitory input is powerful enough to completely eliminate the excitatory action of the afferent nerve but is ineffective regarding other excitatory inputs. These observations can be explained by the location and efficiency of the synapses. We conclude that the afferent nerve provides powerful and reliable excitatory input as well as a feed-forward inhibitory input, which is partially presynaptic in origin. These results question the cellular location within the DON where cancelation of expected incoming signals occurs.
Highlights
A wide range of exteroceptive sensory modalities are mediated by hair cells
Stimulating the afferent nerve usually evoked biphasic responses where a depolarizing synaptic potential was followed by a hyperpolarizing response
In the discussion we focus on the four main findings: (a) the low afferent convergence on ascending efferent neurons (AENs), (b) the electrotonic separation of the afferent input from the parallel fibers input in AENs, (c) the unusual voltage dependence of afferent EPSPs in AENs and (d) the properties and mechanisms of the feed-forward inhibition
Summary
A wide range of exteroceptive sensory modalities are mediated by hair cells. The persistently high afferent impulse rate poses special requirements on the recipient synaptic machinery such as high transmission fidelity as well as efficient integrative capabilities. The high impulse rate of this nerve encodes the level of external electric field (Tricas and New, 1998). Unlike other exteroceptive sensory modalities, the ampullary afferents project exclusively to the Dorsal Octavolateral Nucleus (DON) to excite the principal ascending efferent neurons (AENs) as well as interneurons that provide the principal neurons with feed-forward inhibition (Duman, 1997; Oertel and Young, 2004; Biesdorf et al, 2008). Accumulating evidence suggests that the internal circuitry within the DON provides the mechanism that can discriminate between external and self-generated electric fields. Most of the studies are based on unit recordings from intact system that accurately represent the responses of the neurons, are inadequate to examine synaptic mechanisms that are an essential step toward understanding how AENs integrate the electrosensory inputs
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