Plasticity in an electrosensory system. I. General features of a dynamic sensory filter

1. In this study we describe 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 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 that affects the entire fish, or with proprioceptive stimuli. 2. The mechanism by which responses to repetitive afferent inputs are canceled relies on the central generation of "negative image inputs" that 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 of afferent input patterns. 3. These electric fish commonly experience repetitive electrosensory signals as a result of changes in posture. Because 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 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 for > 30 min. 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 6,7-dinitroquinoxaline-2,3-dione 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 stimuli.