Excitatory and inhibitory synaptic mechanisms at the first stage of integration in the electroreception system of the shark

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.

Cerebellum Lecture: the Cerebellar Nuclei—Core of the Cerebellum

“…While lampreys and hagfish lack a cerebellum, they nevertheless have sophisticated cerebellar-like circuitry in the hindbrain for processing signals from the vestibular and lateral line systems. Such cerebellar-like circuits are found throughout the vertebrate lineage, processing a range of sensory information from electrosensation (e.g., the dorsal octavolateral nuclei processing inputs from the ampullae of Lorenzini in sharks and rays; [ 416 ]) to sound (e.g., birds and reptiles [ 417 ]). Like the true cerebellum, cerebellar-like structures are adaptive filters and possess granule-like cells that project parallel axons that synapse orthogonal to dendrites of PC-like, principal output cells [ 418 ].…”

Electroreception in marine fishes: chondrichthyans

“…More recently, Rotem et al . (, ) used a novel in vitro preparation in the bigeye houndshark Iago omanensis (Norman 1939) to investigate the response of the AENs to bioelectric stimuli and discern how stimuli are processed within the DON. This work highlights the importance of understanding how the chondrichthyan electrosensory system filters and integrates information without the efferent innervation that modulates the sensory hair cells in the related octavolateral modalities.…”

“…Current evidence suggests that a feed‐forward mechanism is used where the electroreceptor afferents stimulate the highly sensitive primary AEN fibres and the less sensitive secondary fibres that run parallel to the primaries. These secondary fibres in turn use gamma‐aminobutyric acid ( GABA )‐receptor mediated inhibition to eliminate the noise in the primary fibres caused by the respiratory induced signal common to the electroreceptors that have converged upon that particular AEN pathway (Rotem et al, , ).…”