From neural mechanisms to ecology: a neuroethological approach to a novel form of memory

Changes in synaptic strength as a cellular mechanism for the formation of memory, such as Long-Term Potentiation and Depression are intensely studied. However, little is known about how synaptically induced long-term changes in the intrinsic excitability of neurons contribute to memory. Nothing is known about how the quantitative aspects of sensory stimuli are transduced into a graded change in intrinsic excitability and how this modifies the behavior of an animal. In this dissertation I present a novel example of sensorimotor adaptation in the electromotor output of a weakly electric fish. The adaptation is an increase in the electric organ discharge frequency in response to prolonged jamming of the electrosensory system lasting for hours to tens of hours beyond the duration of the stimulus. The adaptation can be characterized as a nonassociative memory process. I demonstrate in a brain slice preparation that the memory is formed in the pacemaker nucleus and that the pacemaker also responds to long-lasting synaptic stimulation with an increase in the postsynaptic spike frequency persisting for hours after stimulus termination. In addition, I show in vivo and in vitro that the memory is graded with stimulus duration and amplitude, and that it is synaptically induced by NMDA receptor activation. The memory is maintained by a change in intrinsic excitability within the pacemaker nucleus and not by a change in network properties, such as a modification of synaptic strength. Moreover, the memory shows species-specific differences in its strength and duration and it correlates with the animal’s social environment. These are the first reports to highlight how a graded long-term change in intrinsic neuronal excitability leads to memory and modifies behavior in a species-specific manner. Sensorimotor adaptation in the electromotor system of weakly electric fish therefore could serve as an important model system for understanding the cellular mechanisms behind memory formation in all vertebrate systems, including humans, and in a classic neuroethological sense, contributes to our understanding how ecology instructs the evolutionary adaptation of neuronal plasticity.