Plasticity in an Electrosensory System III: Contrasting Properties of
Spatially Segregated Dendritic Inputs.
J. Bastian.
Department of Zoology, University of Oklahoma, Norman, OK 73019 USA.
APStracts 4:366N, 1997.
ABSTRACT
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 which 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 which convey descending information to pyramidal cell apical
dendrites. One pathway terminates proximally, nearer to the pyramidal cell
body, while 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 (>ÿ7E8 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 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 IPSPs.
Anti-Hebbian plasticity was demonstrated by pairing tetanic stimulation of
either pathway with changes in the postsynaptic cell's membrane potential.
Following 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.
Received 2 October 1997; accepted in final form 3 December 1997.
APS Manuscript Number J806-7.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1997 The American Physiological Society.
Published in APStracts on 12 December 1997