RESUMO
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.
RESUMO
Learning to predict the component in the sensory information resulting from the organism's own activity enables it to respond appropriately to unexpected stimuli. For example, the elasmobranch dorsal octavolateral nucleus (DON) can apparently extract the unexpected component (i.e. generated by nearby organisms) from the incoming electrosensory signals. Here we introduce a novel and unique experimental approach that combines the advantages of in vitro preparations with the integrity of in vivo conditions. In such an experimental system one can study, under control conditions, the cellular and network mechanisms that underlie cancellation of expected sensory inputs. Using extracellular and intracellular recordings we compared the dynamics and spatiotemporal organization of the electrosensory afferent nerve and parallel fiber inputs to the DON. The afferent nerve has a low threshold and high conduction velocity; a stimulus that recruits a small number of fibers is sufficient to activate the principal neurons. The excitatory postsynaptic potential in the principal cells evoked by afferent nerve fibers has fast kinetics that efficiently reach the threshold for action potential. In contrast, the parallel fibers have low conduction velocity, high threshold and extensive convergence on the principal neurons of the DON. The excitatory postsynaptic response has slow kinetics that provides a wide time window for integration of inputs. The highly efficient connection between the afferent nerve and the principal neurons in the DON indicates that filtration occurring in the DON cannot be mediated simply by summation of the parallel fibers' signals with the afferent sensory signals. Hence we propose that the filtering may be mediated via secondary neurons that adjust the principal neurons' sensitivity to afferent inputs.
