Stimulus encoding and feature extraction by multiple sensory neurons. (1/87)

Neighboring cells in topographical sensory maps may transmit similar information to the next higher level of processing. How information transmission by groups of nearby neurons compares with the performance of single cells is a very important question for understanding the functioning of the nervous system. To tackle this problem, we quantified stimulus-encoding and feature extraction performance by pairs of simultaneously recorded electrosensory pyramidal cells in the hindbrain of weakly electric fish. These cells constitute the output neurons of the first central nervous stage of electrosensory processing. Using random amplitude modulations (RAMs) of a mimic of the fish's own electric field within behaviorally relevant frequency bands, we found that pyramidal cells with overlapping receptive fields exhibit strong stimulus-induced correlations. To quantify the encoding of the RAM time course, we estimated the stimuli from simultaneously recorded spike trains and found significant improvements over single spike trains. The quality of stimulus reconstruction, however, was still inferior to the one measured for single primary sensory afferents. In an analysis of feature extraction, we found that spikes of pyramidal cell pairs coinciding within a time window of a few milliseconds performed significantly better at detecting upstrokes and downstrokes of the stimulus compared with isolated spikes and even spike bursts of single cells. Coincident spikes can thus be considered "distributed bursts." Our results suggest that stimulus encoding by primary sensory afferents is transformed into feature extraction at the next processing stage. There, stimulus-induced coincident activity can improve the extraction of behaviorally relevant features from the stimulus.  (+info)

Dynamically interacting processes underlie synaptic plasticity in a feedback pathway. (2/87)

Descending feedback is a common feature of sensory systems. Characterizing synaptic plasticity in feedback inputs is essential for delineating the role of feedback in sensory processing. In this study, we demonstrate that multiple interacting processes underlie the dynamics of synaptic potentiation in one such sensory feedback pathway. We use field recording and modeling to investigate the interaction between the transient high-magnitude potentiation (200-300%) elicited during tetanic stimulation of the feedback pathway and the lower magnitude posttetanic potentiation (PTP; ~30%) that slowly decays on cessation of the tetanus. The amplitude of the observed transient potentiation is graded with stimulus frequency. In contrast, the induction of PTP has a stimulus frequency threshold between 1 and 5 Hz, and its amplitude is independent of stimulus frequency. We suggest that the threshold for PTP induction may be linked to a minimum level of sustained potentiation (MSP) during repetitive trains of stimuli. We have developed a novel model that describes the interaction between the transient plasticity observed during train stimulation and the generation of PTP. The model combines a multiplicative, facilitation-depression-type (FD) model that describes the transient plasticity, with an enzymatic network that describes the dynamics of PTP. The model links transient plasticity to PTP through an input term that reflects MSP. The stratum fibrosum-pyramidal cell (StF-PC) synapse investigated in this study is the terminus of a feedback pathway to the electrosensory lateral line lobe (ELL) of a weakly electric gymnotiform fish. Dynamic plasticity at the StF-PC synapse may contribute to the putative role of this feedback pathway as a sensory searchlight.  (+info)

Sensitivity to novel feedback at different phases of a gymnotid electric organ discharge. (3/87)

Weakly electric fish communicate and electrolocate objects in the dark by discharging their electric organs (EOs) and monitoring the spatiotemporal pattern of current flow through their skin. In the South-American pulse-type gymnotid fish these organs often are intriguingly complex, comprising several hundreds of electrogenic cells (electrocytes) of various morphologies, innervation patterns and abilities to generate a spike, distributed over nearly the full length of the fish. An attractive idea is that different parts of the organ may serve distinct functions in electrocommunication and electrolocation. Recent studies support this notion and suggest that the currents produced during the final phase of the electric organ discharge (EOD) are used for communication. Here, we explore a method to directly assess the relevance of the various currents for electrolocation. In this new method, the pattern of current flow during a gymnotid EOD is changed selectively at distinct phases of the EOD so that currents generated by known electrocyte groups are affected. We have studied the roles played by the various currents for the detection of novel feedback at the trunk/tail region of the gymnotid fish Gymnotus carapo. An experimental animal rested in a cage and two electrodes were placed at a close distance to its trunk and tail. An electronic switch briefly connected these electrodes during a selected phase within an EOD and the shunting of EOD current that resulted from switch closure was directly monitored. G. carapo responded with an acceleration of its discharge rate to novelties in the EOD feedback that occurred only for a fraction of a single EOD. Controls in which the switch was closed during the silent intervals between successive EODs showed that the fish responded to the changes in EOD feedback and not to unrelated artefacts of the brief switch closure. Fish responded to shunting of current during all phases; the sensitivity was highest during the final headnegative phase but the magnitude of shunted current was largest in the preceeding phase. The current produced during the final part of the EOD is thus not reserved for communication as previously suggested but plays a predominant role in electrolocation at the trunk and tail region of G. carapo.  (+info)

Dynamics of electrosensory feedback: short-term plasticity and inhibition in a parallel fiber pathway. (4/87)

The dynamics of neuronal feedback pathways are generally not well understood. This is due to the complexity arising from the combined dynamics of closed-loop feedback systems and the synaptic plasticity of feedback connections. Here, we investigate the short-term synaptic dynamics underlying the parallel fiber feedback pathway to a primary electrosensory nucleus in the weakly electric fish, Apteronotus leptorhynchus. In open-loop conditions, the dynamics of this pathway arise from a monosynaptic excitatory connection and a disynaptic (feed-forward) inhibitory connection to pyramidal neurons in the electrosensory lateral line lobe (ELL). In a brain slice preparation of the ELL, we characterized the synaptic responses of pyramidal neurons to short trains of electrical stimuli delivered to the parallel fibers of the dorsal molecular layer. Stimulus trains consisted of 20 pulses, at either random intervals or constant intervals, with varying mean frequencies. With random trains, pyramidal neuron responses were well described by a single exponential function of the inter-stimulus interval-suggesting a single facilitation-like process underlies these synaptic dynamics. However, responses to periodic (constant interval) trains deviated from this simple description. Random and periodic stimulus trains delivered when the feed-forward inhibitory component of this pathway was pharmacologically blocked revealed that inhibition and depression also contribute to the observed dynamics. We formulated a simple model of the parallel fiber synaptic dynamics that provided an accurate description of our data. The model dynamics resulted from a combination of three distinct processes. Two of the processes are the classically-described synaptic facilitation and depression, and the third is a novel description of feed-forward inhibition. An analysis of this model suggests that synaptic pathways combining plasticity with feed-forward inhibition can be easily tuned to signal different types of transient stimuli and thus lead to diverse and nonintuitive filtering properties.  (+info)

Electroreception in G carapo: detection of changes in waveform of the electrosensory signals. (5/87)

Electric fish evaluate the near environment by detecting changes in their self-generated electric organ discharge. To investigate impedance modulation of the self-generated electric field, this field was measured at the electrosensory fovea of Gymnotus carapo in the presence and absence of objects. Changes in local fields provoked by resistive objects were predicted by the change in total energy. Objects with capacitive impedance generated large variations in the relative importance of the different waveform components of the electric organ discharge. We tested the hypothesis that fish discriminate changes in waveform as well as increases in total energy using the novelty response, which is a behavioural response consisting of a transient acceleration of EOD frequency that can follow a change in object impedance. For resistive loads, the amplitude of novelty responses was well predicted by the increase in total energy. For complex loads, the amplitude of novelty responses was correlated not only with increases in total energy but also with waveform changes, consisting of reductions in the early slow negative wave and increases in the late sharp negative wave. The total energy and waveform effects appeared to be additive. These results indicate that G. carapo discriminates complex impedance based on an evaluation of different waveform parameters.  (+info)

Probability and amplitude of novelty responses as a function of the change in contrast of the reafferent image in G carapo. (6/87)

Pulse electric fish evaluate successive electrosensory images generated by self-emitted electric discharges, creating a neural representation of the physical world. Intervals between discharges (system resolution) are controlled by a pacemaker nucleus under the influence of reafferent signals. Novel sensory stimuli cause transient accelerations of the pacemaker rate (novelty responses). This study describes quantitatively the effect of changes in contrast of reafferent electrosensory signals on the amplitude and probability of novelty responses. We found that: (i). alterations of a single image in an otherwise homogeneous series cause a novelty response; (ii). the amplitude of the elicited novelty response is a linear function of the logarithm of the change in image contrast; (iii). the parameters of this function, threshold and proportionality constant, allowed us to evaluate the transference function between change in stimulus amplitude and the amplitude of the novelty response; (iv). both parameters are independent of the baseline contrast; (v). the proportionality constant increases with the moving average of the contrast of hundreds of previous images. These findings suggest that the electrosensory system (i). calculates the difference between each reafferent electrosensory image and a neural representation of the past electrosensory input ('template'); (ii). creates the comparison template in which the relative contribution of every image decreases with the incorporation of successive images. We conclude that contrast discrimination in the electrosensory system of G. carapo obeys the general principle of appreciating any instantaneous input by the input's departure from a moving average of past images.  (+info)

A dynamic dendritic refractory period regulates burst discharge in the electrosensory lobe of weakly electric fish. (7/87)

Na+-dependent spikes initiate in the soma or axon hillock region and actively backpropagate into the dendritic arbor of many central neurons. Inward currents underlying spike discharge are offset by outward K+ currents that repolarize a spike and establish a refractory period to temporarily prevent spike discharge. We show in a sensory neuron that somatic and dendritic K+ channels differentially control burst discharge by regulating the extent to which backpropagating dendritic spikes can re-excite the soma. During repetitive discharge a progressive broadening of dendritic spikes promotes a dynamic increase in dendritic spike refractory period. A leaky integrate-and-fire model shows that spike bursts are terminated when a decreasing somatic interspike interval and an increasing dendritic spike refractory period synergistically act to block backpropagation. The time required for the somatic interspike interval to intersect with dendritic refractory period determines burst frequency, a time that is regulated by somatic and dendritic spike repolarization. Thus, K+ channels involved in spike repolarization can efficiently control the pattern of spike output by establishing a soma-dendritic interaction that invokes dynamic shifts in dendritic spike properties.  (+info)

Serotonin modulates the electric waveform of the gymnotiform electric fish Brachyhypopomus pinnicaudatus. (8/87)

The gymnotiform electric fish Brachyhypopomus pinnicaudatus communicates with a sexually dimorphic electric waveform, the electric organ discharge (EOD). Males display pronounced circadian rhythms in the amplitude and duration of their EODs. Changes in the social environment influence the magnitudes of these circadian rhythms and also produce more transient responses in the EOD waveforms. Here we show that injections of serotonin produce quick, transient, dose-dependent enhancements of the male EOD characters similar to those induced by encounters with another male. The response to serotonin administered peripherally begins 5-10 min post injection and lasts approximately 3 h. The magnitude of the response to serotonin is tightly associated with the magnitude of the day-to-night swing of the circadian rhythm prior to injection. Taken together these findings suggest that the male's social environment influences his response to serotonin by altering the function of some part of the downstream chain between the serotonin receptors and the ion channels involved in control of the EOD waveform. Although chronic activation of serotonin circuitry is widely known to elicit subordinate behavior, we find that 5-HT initially increases a dominance signal in these fish. These findings are consistent with the emerging view that serotonin facilitates different adaptive responses to acute and chronic social challenge and stress.  (+info)