Plasticity in an electrosensory system. II. Postsynaptic events associated with a dynamic sensory filter

Abstract

1. This report summarizes studies of the changes in postsynaptic potentials that occur as pyramidal cells within the primary electrosensory processing nucleus learn to reject repetitive patterns of afferent input. The rejection mechanism employs "negative image inputs" that oppose or cancel electroreceptor afferent inputs or patterns of pyramidal hyperpolarization or depolarization caused by intracellular current injection. Feedback pathways carrying descending electrosensory as well as other types of information provide the negative image inputs. This study focuses on the role of a directly descending projection from a second-order electrosensory nucleus the nucleus praeeminentialis (nP), which provides excitatory and inhibitory inputs to the apical dendrites of electrosensory lateral line lobe (ELL) pyramidal cells. 2. Electrical stimulation of the pathway linking the nP to the ELL was used to activate descending inputs to the pyramidal cells. Pyramidal cell activity was typically increased due to stimulation of this pathway. Tetanic stimulation of the descending pathway paired with either electrosensory stimuli that inhibited pyramidal cells, or hyperpolarizing current injection, increased the excitation provided by subsequent stimulation of this pathway. Pairing tetanic stimulation with excitatory electrosensory stimuli or depolarizing current injection had the opposite effect. Subsequent activation of the descending pathway inhibited pyramidal cells. 3. Intracellular recordings showed that the increased firing of pyramidal cells evoked by stimulation of the descending pathway following tetanic stimulation paired with postsynaptic hyperpolarization resulted from larger amplitude and longer-duration excitatory postsynaptic potentials (EPSPs). The shift in the effect of activity in this descending pathway to providing net inhibitory input to the pyramidal cells after paired presynaptic activity and postsynaptic depolarization probably results from the potentiation of inhibitory postsynaptic potentials (IPSPs). The EPSP and IPSPs evoked by activity in this descending pathway can be continuously adjusted in amplitude, thereby counterbalancing patterns of pyramidal cell excitation and inhibition received from the periphery with the result that repetitive patterns of afferent activity are strongly attenuated.