Plasticity in an Electrosensory system I: General Features of a Dynamic
Department of Zoology, University of Oklahoma, Norman, OK 73019, USA.
APStracts 3:0103N, 1996.
SUMMARY AND CONCLUSIONS
1. This study describes changes in neuronal responses within the primary
electrosensory processing nucleus of a weakly electric fish that occur when
the fish are exposed to repetitive patterns of electrosensory stimuli.
Extracellular single unit recordings show that pyramidal cells within the
electrosensory lateral line lobe (ELL) develop, over a time course of several
minutes, an insensitivity to repetitive stimuli applied to a cell's receptive
field (local stimulus). The pyramidal cell response cancellation only develops
if the local stimulus is applied simultaneously with a diffuse pattern of
electrosensory stimulation which affects the entire fish, or with
proprioceptive stimuli. 2. The mechanism by which responses to repetitive
afferent inputs are canceled relies upon the central generation of "negative
image inputs" which provide increased inhibitory input to a cell's apical
dendrites at times when excitatory afferent input is increased. The negative
image input becomes excitatory when afferent excitation is reduced or when
input from inhibitory interneurons is predominant. The integration of a
specific pattern of receptor afferent input with the complementary negative
image input results in strong attenuation of pyramidal cell responses. The
negative image inputs are plastic so that a single pyramidal cell can learn to
reject a variety afferent input patterns. 3. These electric fish commonly
experience repetitive electrosensory signals as a result of changes in
posture. Since the electric organ is located in the trunk and tail, cyclical
movements associated with exploratory behaviors result in amplitude
modulations (AMs) of the electric field and these AMs alter electroreceptor
afferent firing frequency but not the firing frequency of second-order
pyramidal cells. The adaptive cancellation mechanism described in this study
can account for the insensitivity of pyramidal cells to reafferent
electrosensory stimulation caused by tail movements and other postural
changes. 4. The tail movements generate proprioceptive as well as
electrosensory inputs and either of these signals alone provides sufficient
information for the generation of negative image inputs. The size of the
negative image input is larger, however, if both inputs are active.
5. The synaptic plasticity underlying the development of negative image inputs
has a long-term component; under appropriate conditions changes in synaptic
efficacy persist in excess of 30 minutes. 6. Normally functioning
glutamatergic synapses are necessary for the expression of the synaptic
plasticity associated with this cancellation mechanism. The development of
negative image responses is blocked by micropressure ejection of the glutamate
antagonist DNQX into the neighborhood of the pyramidal cell apical dendrites.
7. The adaptive cancellation of repetitive inputs is based on anti-Hebbian
mechanisms; that is, correlated pre and postsynaptic activity lead to a
reduction in the excitatory input provided by the plastic synapses. As has
been shown for several other systems, the cancellation mechanism reduces the
cells' responses to reafferent patterns of sensory input. In addition, the
results of this study indicate that the mechanism may be more general,
enabling the system to also cancel patterns of input resulting from exogenous
Received 25 March 1996; accepted in final form 21 May 1996.
APS Manuscript Number J243-6.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 5 June 96