Plasticity in an electrosensory system. III. Contrasting properties of spatially segregated dendritic inputs.

Efferent neurons of the first-order electrosensory processing center of the brain, the electrosensory lateral line lobe (ELL), receive electroreceptor afferent input as well as feedback inputs descending from higher centers. These ELL efferents, pyramidal cells, adaptively filter predictable patterns of sensory input while preserving sensitivity to novel stimuli. The filter mechanism involves integration of centrally generated predictive inputs with the afferent inputs being canceled. The predictive inputs, referred to as "negative image" inputs, terminate on pyramidal cell apical dendrites and generate responses that are opposite those resulting from the predictable afference, hence integration of these signals results in attenuation of pyramidal cell responses. The system also shows a robust form of plasticity; the pyramidal cells learn, with a time course of a few minutes, to cancel new patterns of repetitive inputs. This is accomplished by adjusting the strength of excitatory and inhibitory apical dendritic inputs according to an anti-Hebbian learning rule. This study focuses on the properties of two separate pathways that convey descending information to pyramidal cell apical dendrites. One pathway terminates proximally, nearer to the pyramidal cell body, whereas the other terminates distally. Recordings of ELL evoked potentials, extracellular pyramidal cell spike responses, and intracellularly recorded synaptic potentials show that the pyramidal cells respond oppositely to moderate-frequency (> approximately 8 Hz) single pulse stimulation or repeated (1/s) tetanic activation of these two pathways. Repetitive activation of the proximally terminating pathway results in highly facilitating responses due to potentiation of pyramidal cell excitatory postsynaptic potentials (EPSPs). These same stimuli applied to the distally terminating pathway result in a reduction of pyramidal cell responses due to depression of EPSPs and potentiation of inhibitatory postsynaptic potentials (IPSPs). Anti-Hebbian plasticity was demonstrated by pairing tetanic stimulation of either pathway with changes in the postsynaptic cell's membrane potential. After stabilization of the response potentiation due to tetanic stimulation of the proximally terminating pathway, paired postsynaptic hyperpolarization resulted in further increases in spike responses and additional potentiation of pyramidal cell EPSPs. Paired postsynaptic depolarization reduced subsequent responses to the tetanus, depressed EPSP amplitudes, and, in many cases, potentiated IPSPs. The same pattern of plasticity was observed when postsynaptic hyper- or depolarization was paired with tetanic stimulation of the distally terminating pathway except that the plasticity was superimposed on the depressed pyramidal cell responses resulting from stimulating this pathway alone. Modulation of a postsynaptic form of synaptic depression is proposed to account for the anti-Hebbian plasticity associated with both pathways.