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Journal of Neurophysiology, Vol 76, Issue 4 2483-2496, Copyright © 1996 by APS
ARTICLES |
J. Bastian
Department of Zoology, University of Oklahoma, Norman 73019, USA.
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.
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A.-M. M. Oswald, M. J. Chacron, B. Doiron, J. Bastian, and L. Maler Parallel Processing of Sensory Input by Bursts and Isolated Spikes J. Neurosci., May 5, 2004; 24(18): 4351 - 4362. [Abstract] [Full Text] [PDF]
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E. Harvey-Girard and R. J. Dunn Excitatory Amino Acid Receptors of the Electrosensory System: The NR1/NR2B N-Methyl-D-Aspartate Receptor J Neurophysiol, February 1, 2003; 89(2): 822 - 832. [Abstract] [Full Text] [PDF]
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A.-M. M. Oswald, J. E. Lewis, and L. Maler Dynamically Interacting Processes Underlie Synaptic Plasticity in a Feedback Pathway J Neurophysiol, May 1, 2002; 87(5): 2450 - 2463. [Abstract] [Full Text] [PDF]
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J. Bastian and J. Nguyenkim Dendritic Modulation of Burst-Like Firing in Sensory Neurons J Neurophysiol, January 1, 2001; 85(1): 10 - 22. [Abstract] [Full Text] [PDF]
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 C Assad, B Rasnow, and P. Stoddard Electric organ discharges and electric images during electrolocation J. Exp. Biol., January 5, 1999; 202(10): 1185 - 1193. [Abstract] [PDF]
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N. Berman and L Maler Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering J. Exp. Biol., January 5, 1999; 202(10): 1243 - 1253. [Abstract] [PDF]
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R. Turner and L Maler Oscillatory and burst discharge in the apteronotid electrosensory lateral line lobe J. Exp. Biol., January 5, 1999; 202(10): 1255 - 1265. [Abstract] [PDF]
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J Bastian Plasticity of feedback inputs in the apteronotid electrosensory system J. Exp. Biol., January 5, 1999; 202(10): 1327 - 1337. [Abstract] [PDF]
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C. Bell, V. Han, Y Sugawara, and K Grant Synaptic plasticity in the mormyrid electrosensory lobe J. Exp. Biol., January 5, 1999; 202(10): 1339 - 1347. [Abstract] [PDF]
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N. J. Berman and L. Maler Inhibition Evoked From Primary Afferents in the Electrosensory Lateral Line Lobe of the Weakly Electric Fish (Apteronotus leptorhynchus) J Neurophysiol, December 1, 1998; 80(6): 3173 - 3196. [Abstract] [Full Text] [PDF]
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N. J. Berman and L. Maler Interaction of GABAB-Mediated Inhibition With Voltage-Gated Currents of Pyramidal Cells: Computational Mechanism of a Sensory Searchlight J Neurophysiol, December 1, 1998; 80(6): 3197 - 3213. [Abstract] [Full Text] [PDF]
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J. Bastian Modulation of Calcium-Dependent Postsynaptic Depression Contributes to an Adaptive Sensory Filter J Neurophysiol, December 1, 1998; 80(6): 3352 - 3355. [Abstract] [Full Text] [PDF]
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D. Bottai, L. Maler, and R. J. Dunn Alternative RNA Splicing of the NMDA Receptor NR1 mRNA in the Neurons of the Teleost Electrosensory System J. Neurosci., July 15, 1998; 18(14): 5191 - 5202. [Abstract] [Full Text] [PDF]
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J. Bastian Plasticity in an Electrosensory System. III. Contrasting Properties of Spatially Segregated Dendritic Inputs J Neurophysiol, April 1, 1998; 79(4): 1839 - 1857. [Abstract] [Full Text] [PDF]
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D. Wang and L. Maler In Vitro Plasticity of the Direct Feedback Pathway in the Electrosensory System of Apteronotus leptorhynchus J Neurophysiol, October 1, 1997; 78(4): 1882 - 1889. [Abstract] [Full Text] [PDF]
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