Electrosensory Lateral Line Lobe Research Articles

Sparse and dense coding of natural stimuli by distinct midbrain neuron subpopulations in weakly electric fish

While peripheral sensory neurons respond to natural stimuli with a broad range of spatiotemporal frequencies, central neurons instead respond sparsely to specific features in general. The nonlinear transformations leading to this emergent selectivity are not well understood. Here we characterized how the neural representation of stimuli changes across successive brain areas, using the electrosensory system of weakly electric fish as a model system. We found that midbrain torus semicircularis (TS) neurons were on average more selective in their responses than hindbrain electrosensory lateral line lobe (ELL) neurons. Further analysis revealed two categories of TS neurons: dense coding TS neurons that were ELL-like and sparse coding TS neurons that displayed selective responses. These neurons in general responded to preferred stimuli with few spikes and were mostly silent for other stimuli. We further investigated whether information about stimulus attributes was contained in the activities of ELL and TS neurons. To do so, we used a spike train metric to quantify how well stimuli could be discriminated based on spiking responses. We found that sparse coding TS neurons performed poorly even when their activities were combined compared with ELL and dense coding TS neurons. In contrast, combining the activities of as few as 12 dense coding TS neurons could lead to optimal discrimination. On the other hand, sparse coding TS neurons were better detectors of whether their preferred stimulus occurred compared with either dense coding TS or ELL neurons. Our results therefore suggest that the TS implements parallel detection and estimation of sensory input.

Are mushroom bodies cerebellum-like structures?

The mushroom bodies are distinctive neuropils in the protocerebral brain segments of many protostomes. A defining feature of mushroom bodies is their intrinsic neurons, masses of cytoplasm-poor globuli cells that form a system of lobes with their densely-packed, parallel-projecting axon-like processes. In insects, the role of the mushroom bodies in olfactory processing and associative learning and memory has been studied in depth, but several lines of evidence suggest that the function of these higher brain centers cannot be restricted to these roles. The present account considers whether insight into an underlying function of mushroom bodies may be provided by cerebellum-like structures in vertebrates, which are similarly defined by the presence of masses of tiny granule cells that emit thin parallel fibers forming a dense molecular layer. In vertebrates, the shared neuroarchitecture of cerebellum-like structures has been suggested to underlie a common functional role as adaptive filters for the removal of predictable sensory elements, such as those arising from reafference, from the total sensory input. Cerebellum-like structures include the vertebrate cerebellum, the electrosensory lateral line lobe, dorsal and medial octavolateral nuclei of fish, and the dorsal cochlear nucleus of mammals. The many architectural and physiological features that the insect mushroom bodies share with cerebellum-like structures suggest that it might be fruitful to consider mushroom body function in light of a possible role as adaptive sensory filters. The present account thus presents a detailed comparison of the insect mushroom bodies with vertebrate cerebellum-like structures.

Routing the Flow of Sensory Signals Using Plastic Responses to Bursts and Isolated Spikes: Experiment and Theory

Processing complex sensory environments efficiently requires a diverse array of neural coding strategies. Neural codes relying on specific temporal patterning of action potentials may offer advantages over using solely spike rate codes. In particular, stimulus-dependent burst firing may carry additional information that isolated spikes do not. We use the well characterized electrosensory system of weakly electric fish to address how stimulus-dependent burst firing can determine the flow of information in feedforward neural circuits with different forms of short-term synaptic plasticity. Pyramidal cells in the electrosensory lateral line lobe burst in response to low-frequency, local (prey) signals. We show that the ability of pyramidal cells to code for local signals in the presence of additional high-frequency, global (communication) stimuli is uncompromised, while burst firing is reduced. We developed a bursting neuron model to understand how these effects, in particular noise-induced burst suppression, arise from interplay between incoming sensory signals and intrinsic neuronal dynamics. Finally, we examined how postsynaptic target populations preferentially respond to one of the two sensory mixtures (local vs local plus global) depending on whether the populations are in receipt of facilitating or depressing synapses. This form of feedforward neural architecture may allow for efficient information flow in the same neural pathway via either isolated or burst spikes, where the mechanisms by which stimuli are encoded are adaptable and sensitive to a diverse array of stimulus and contextual mixtures.

Environmental complexity, seasonality and brain cell proliferation in a weakly electric fish, Brachyhypopomus gauderio

Environmental complexity and season both influence brain cell proliferation in adult vertebrates, but their relative importance and interaction have not been directly assessed. We examined brain cell proliferation during both the breeding and non-breeding seasons in adult male electric fish, Brachyhypopomus gauderio, exposed to three environments that differed in complexity: (1) a complex natural habitat in northern Uruguay, (2) an enriched captive environment where fish were housed socially and (3) a simple laboratory setting where fish were isolated. We injected fish with BrdU 2.5 h before sacrifice to label newborn cells. We examined the hindbrain and midbrain and quantified the density of BrdU+ cells in whole transverse sections, proliferative zones and two brain nuclei in the electrocommunication circuitry (the pacemaker nucleus and the electrosensory lateral line lobe). Season had the largest effect on cell proliferation, with fish during the breeding season having three to seven times more BrdU+ cells than those during the non-breeding season. Although the effect was smaller, fish from a natural environment had greater rates of cell proliferation than fish in social or isolated captive environments. For most brain regions, fish in social and isolated captive environments had equivalent levels of cell proliferation. However, for brain regions in the electrocommunication circuitry, group-housed fish had more cell proliferation than isolated fish, but only during the breeding season (season × environment interaction). The regionally and seasonally specific effect of social environment on cell proliferation suggests that addition of new cells to these nuclei may contribute to seasonal changes in electrocommunication behavior.

Inhibition of SK and M channel-mediated currents by 5-HT enables parallel processing by bursts and isolated spikes.

Although serotonergic innervation of sensory brain areas is ubiquitous, its effects on sensory information processing remain poorly understood. We investigated these effects in pyramidal neurons within the electrosensory lateral line lobe (ELL) of weakly electric fish. Surprisingly, we found that 5-HT is present at different levels across the different ELL maps; the presence of 5-HT fibers was highest in the map that processes intraspecies communication signals. Electrophysiological recordings revealed that 5-HT increased excitability and burst firing through a decreased medium afterhyperpolarization resulting from reduced small-conductance calcium-activated (SK) currents as well as currents mediated by an M-type potassium channel. We next investigated how 5-HT alters responses to sensory input. 5-HT application decreased the rheobase current, increased the gain, and decreased first spike latency. Moreover, it reduced discriminability between different stimuli, as quantified by the mutual information rate. We hypothesized that 5-HT shifts pyramidal neurons into a burst-firing mode where bursts, when considered as events, can detect the presence of particular stimulus features. We verified this hypothesis using signal detection theory. Our results indeed show that serotonin-induced bursts of action potentials, when considered as events, could detect specific stimulus features that were distinct from those detected by isolated spikes. Moreover, we show the novel result that isolated spikes transmit more information after 5-HT application. Our results suggest a novel function for 5-HT in that it enables differential processing by action potential patterns in response to current injection.

Neural Heterogeneity and Efficient Population Codes for Communication Signals

Efficient sensory coding implies that populations of neurons should represent information-rich aspects of a signal with little redundancy. Recent studies have shown that neural heterogeneity in higher brain areas enhances the efficiency of encoding by reducing redundancy across the population. Here, we study how neural heterogeneity in the early stages of sensory processing influences the efficiency of population codes. Through the analysis of in vivo recordings, we contrast the encoding of two types of communication signals of electric fishes in the most peripheral sensory area of the CNS, the electrosensory lateral line lobe (ELL). We show that communication signals used during courtship (big chirps) and during aggressive encounters (small chirps) are encoded by different populations of ELL pyramidal cells, namely I-cells and E-cells, respectively. Most importantly, we show that the encoding strategy differs for the two signals and we argue that these differences allow these cell types to encode specifically information-rich features of the signals. Small chirps are detected, and their timing is accurately signaled through stereotyped spike bursts, whereas the shape of big chirps is accurately represented by variable increases in firing rate. Furthermore, we show that the heterogeneity across I-cells enhances the efficiency of the population code and thus permits the accurate discrimination of different quality courtship signals. Our study shows the importance of neural heterogeneity early in a sensory system and that it initiates the sparsification of sensory representation thereby contributing to the efficiency of the neural code.

Spatial stimulation of the electrosensory system of mormyrid electric fish

The long-term goal of this project is to understand adaptive processing in sensory systems. Our work focuses on the electrosensory system of the mormyrid electric fish, a system uniquely suited for the study of adaptive sensory processing. The electrosensory lateral line lobe (ELL) of the mormyrid electric fish presents a special opportunity for examining the influence adaptation on sensory processing because much of the physiology [1] and anatomy [2] has been well characterized. The mormyrid electric fish senses its environment by emitting an electric organ discharge (EOD) and detecting the perturbations that nearby objects cause in the self-generated electric field. Specialized mormyromast electroreceptors sense the self-generated field and its distortions. Afferent fibers from these electroreceptors respond to the fish’s own EOD, and the field strength of the electric field is encoded in the latency of the afferent spike response [3,4]. The electrosensory responses are conveyed with somatotopic precision to the ELL where the fibers terminate [5]. Previous research on electrosensory adaptation has concentrated on point-like electrical fields on the skin. Since the purpose of the electrosensory system is to analyze changes in spatial patterns, we expect that presenting a spatially distributed electrical pattern will lead to a better understanding of adaptive aspects of electrosensory processing in ELL. Thus, we have begun construction of a stimulus device that can present a spatially distributed electrical pattern on the skin of a mormyrid fish. By controlling the patterns that we present, we can simultaneously record from principal cells of ELL to observe changes in responses to spatial patterns. The first phase of our stimulus development program has been to present a low-resolution, 1-dimensional pattern on the fish’s skin. The design was based on an array of vertical rectangles that could be independently controlled to present a spatially varying electrical image along the fish’s skin. We developed electrostatic models to predict fields that would be generated by an array of stimulator pads in water. We have developed an electrical pattern design algorithm that will approximate any given electrical pattern by imposing a set of electrical potentials on the stimulator array. The algorithm will allow flexibility in electrophysiological experimental design to test hypotheses about spatial effects on sensory processing. A cellular modeling component of this study has been developed to predict the responses of individual neurons to stimulation by spatial patterns. Results of our neuronal network models will be compared with experimental measurements of cell responses to the same stimulation to iteratively improve our understanding of mechanisms of electrosensory processing.

Coding signal strength by correlated activity in bursting neurons

Understanding how populations of neurons encode sensory information is of critical importance [1]. Correlations between the activities of neurons are ubiquitous in the central nervous system and, although their implications for encoding and decoding of sensory information has been the subject of arduous debates, there is a general consensus that their effects can be significant [2]. As such, there is great interest in understanding how correlated activity can be regulated. Recent experimental evidence has shown that correlated activity amongst pyramidal cells within the electrosensory lateral line lobe (ELL) of weakly electric fish can be regulated based on the behavioral context: these cells modulate their correlated activity depending on whether the fish is performing electrolocation or communication tasks without changing the mean firing rate of their response [3]. Moreover, it was shown in the same study that the changes in correlated activity were correlated with changes in bursting dynamics. In this work we explore the role of intrinsic bursting dynamics on the correlated activity of ELL pyramidal neurons. We use a combination of mathematical modeling as well as in vivo and in vitro electrophysiology to show that bursting dynamics can significantly alter the ability of neuronal populations to be correlated by common input. In particular, our model predicts that the ratio of output to input correlations (i.e. the correlation susceptibility [4]) is largely independent of stimulus amplitude when neurons are in the tonic firing model. In contrast, we find that the correlation susceptibility increases with stimulus amplitude when the neurons are in the bursting mode (Fig. ​(Fig.1).1). We then performed in vivo and in vitro experiments to verify this prediction. Our results show that intrinsic dynamics have important consequences on correlated activity and have further revealed a potential coding mechanism for stimulus amplitude through correlated activity. Figure 1 Modeling results Output correlation coefficient, r, as a function of input correlation, c, for three different stimulus amplitudes in tonic firing neurons A and bursting neurons B. As shown in the inset the correlation susceptibility (i.e. the ratio of ...

Burst-Induced Anti-Hebbian Depression Acts through Short-Term Synaptic Dynamics to Cancel Redundant Sensory Signals

Weakly electric fish can enhance the detection and localization of important signals such as those of prey in part by cancellation of redundant spatially diffuse electric signals due to, e.g., their tail bending. The cancellation mechanism is based on descending input, conveyed by parallel fibers emanating from cerebellar granule cells, that produces a negative image of the global low-frequency signals in pyramidal cells within the first-order electrosensory region, the electrosensory lateral line lobe (ELL). Here we demonstrate that the parallel fiber synaptic input to ELL pyramidal cell undergoes long-term depression (LTD) whenever both parallel fiber afferents and their target cells are stimulated to produce paired burst discharges. Paired large bursts (4-4) induce robust LTD over pre-post delays of up to +/-50 ms, whereas smaller bursts (2-2) induce weaker LTD. Single spikes (either presynaptic or postsynaptic) paired with bursts did not induce LTD. Tetanic presynaptic stimulation was also ineffective in inducing LTD. Thus, we have demonstrated a form of anti-Hebbian LTD that depends on the temporal correlation of burst discharge. We then demonstrated that the burst-induced LTD is postsynaptic and requires the NR2B subunit of the NMDA receptor, elevation of postsynaptic Ca(2+), and activation of CaMKIIbeta. A model incorporating local inhibitory circuitry and previously identified short-term presynaptic potentiation of the parallel fiber synapses further suggests that the combination of burst-induced LTD, presynaptic potentiation, and local inhibition may be sufficient to explain the generation of the negative image and cancellation of redundant sensory input by ELL pyramidal cells.

Neural heterogeneities and stimulus properties affect burst coding in vivo

Many neurons tend to fire clusters of action potentials called bursts followed by quiescence in response to sensory input. While the mechanisms that underlie burst firing are generally well understood in vitro, the functional role of these bursts in generating behavioral responses to sensory input in vivo are less clear. Pyramidal cells within the electrosensory lateral line lobe (ELL) of weakly electric fish offer an attractive model system for studying the coding properties of burst firing, because the anatomy and physiology of the electrosensory circuitry are well understood, and the burst mechanism of ELL pyramidal cells has been thoroughly characterized in vitro. We investigated the coding properties of bursts generated by these cells in vivo in response to mimics of behaviorally relevant sensory input. We found that heterogeneities within the pyramidal cell population had quantitative but not qualitative effects on burst coding for the low frequency components of broadband time varying input. Moreover, spatially localized stimuli mimicking, for example, prey tended to elicit more bursts than spatially global stimuli mimicking conspecific-related stimuli. We also found small but significant correlations between burst attributes such as the number of spikes per burst or the interspike interval during the burst and stimulus attributes such as stimulus amplitude or slope. These correlations were much weaker in magnitude than those observed in vitro. More surprisingly, our results show that correlations between burst and stimulus attributes actually decreased in magnitude when we used low frequency stimuli that are expected to promote burst firing. We propose that this discrepancy is attributable to differences between ELL pyramidal cell burst firing under in vivo and in vitro conditions.

SK Channels Gate Information Processing In Vivo by Regulating an Intrinsic Bursting Mechanism Seen In Vitro

Understanding the mechanistic substrates of neural computations that lead to behavior remains a fundamental problem in neuroscience. In particular, the contributions of intrinsic neural properties such as burst firing and dendritic morphology to the processing of behaviorally relevant sensory input have received much interest recently. Pyramidal cells within the electrosensory lateral line lobe of weakly electric fish display an intrinsic bursting mechanism that relies on somato-dendritic interactions when recorded in vitro: backpropagating somatic action potentials trigger dendritic action potentials that lead to a depolarizing afterpotential (DAP) at the soma. We recorded intracellularly from these neurons in vivo and found firing patterns that were quite different from those seen in vitro: we found no evidence for DAPs as each somatic action potential was followed by a pronounced afterhyperpolarization (AHP). Calcium chelators injected in vivo reduced the AHP, thereby unmasking the DAP and inducing in vitro-like bursting in pyramidal cells. These bursting dynamics significantly reduced the cell's ability to encode the detailed time course of sensory input. We performed additional in vivo pharmacological manipulations and mathematical modeling to show that calcium influx through N-methyl-d-aspartate (NMDA) receptors activate dendritic small conductance (SK) calcium-activated potassium channels, which causes an AHP that counteracts the DAP and leads to early termination of the burst. Our results show that ion channels located in dendrites can have a profound influence on the processing of sensory input by neurons in vivo through the modulation of an intrinsic bursting mechanism.

Receptive field organization across multiple electrosensory maps. II. Computational analysis of the effects of receptive field size on prey localization

The electric fish Apteronotus leptorhynchus emits a high-frequency electric organ discharge (EOD) sensed by specialized electroreceptors (P-units) distributed across the fish's skin. Objects such as prey increase the amplitude of the EOD over the underlying skin and thus cause an increase in P-unit discharge. The resulting localized intensity increase is called the electric image and is detected by its effect on the P-unit population; the electric image peak value and the extent to its spreads are cues utilized by these fish to estimate the location and size of its prey. P-units project topographically to three topographic maps in the electrosensory lateral line lobe (ELL): centromedial (CMS), centrolateral (CLS), and lateral (LS) segments. In a companion paper I have calculated the receptive fields (RFs) in these maps: RFs were small in CMS and very large in LS, with intermediate values in CLS. Here I use physiological data to create a simple model of the RF structure within the three ELL maps and to compute the response of these model maps to simulated prey. The Fisher information (FI) method was used to compute the optimal estimates possible for prey localization across the three maps. The FI predictions were compared with behavioral studies on prey detection. These comparisons were used to frame alternative hypotheses on the functions of the three maps and on the constraints that RF size and synaptic strength impose on weak signal detection and estimation.

Receptive field organization across multiple electrosensory maps. I. Columnar organization and estimation of receptive field size

The electric fish Apteronotus leptorhynchus emits a high-frequency electric organ discharge (EOD) sensed by specialized electroreceptors (P-units). Amplitude modulations (AMs) of the EOD are caused by objects such as prey as well as by social interactions with conspecifics. The firing rate of P-units is modulated by the AMs due to both objects and communication signals. P-units trifurcate as they enter the medulla; they terminate topographically with three maps of the electrosensory lateral line lobe (ELL): the centromedial (CMS), centrolateral (CLS), and lateral (LS) segments. Within each map P-units terminate onto the basal dendrites of pyramidal cells. Anterograde filling of P-units and retrograde filling of the basal bushes of pyramidal cells were used to estimate their respective spreads and spacing in the three maps. These estimates were used to compute the receptive field structure of the pyramidal cells: receptive fields were small in CMS and very large in LS with intermediate values in CLS. There are several classes of pyramidal cells defined by morphological and functional criteria; these cells are organized into columns such that each column contains one member of each class and all cells within a column receive the same P-unit input.

Transient Signals Trigger Synchronous Bursts in an Identified Population of Neurons

It is an important task in neuroscience to find general principles that relate neural codes to the structure of the signals they encode. The structure of sensory signals can be described in many ways, but one important categorization distinguishes continuous from transient signals. We used the communication signals of the weakly electric fish to reveal how transient signals (chirps) can be easily distinguished from the continuous signal they disrupt. These communication signals-low-frequency sinusoids interrupted by high-frequency transients-were presented to pyramidal cells of the electrosensory lateral line lobe (ELL) during in vivo recordings. We show that a specific population of electrosensory neurons encodes the occurrence of the transient signal by synchronously producing a burst of spikes, whereas bursting was neither common nor synchronous in response to the continuous signal. We also confirmed that burst can be triggered by low-frequency modulations typical of prey signals. However, these bursts are more common in a different segment of the ELL and during spatially localized stimulation. These localized stimuli will elicit synchronized bursting only in a restricted number of cells the receptive fields of which overlap the spatial extent of the stimulus. Therefore the number of cells simultaneously producing a burst and the ELL segment responding most strongly may carry the information required to disambiguate chirps from prey signals. Finally we show that the burst response to chirps is due to a biophysical mechanism previously characterized by in vitro studies of electrosensory neurons. We conclude that bursting and synchrony across cells are important mechanisms used by sensory neurons to carry the information about behaviorally relevant but transient signals.

Receptive field properties of neurons in the electrosensory lateral line lobe of the weakly electric fish, Gnathonemus petersii

The receptive field of a sensory neuron is known as that region in sensory space where a stimulus will alter the response of the neuron. We determined the spatial dimensions and the shape of receptive fields of electrosensitive neurons in the medial zone of the electrosensory lateral line lobe of the African weakly electric fish, Gnathonemus petersii, by using single cell recordings. The medial zone receives input from sensory cells which encode the stimulus amplitude. We analysed the receptive fields of 71 neurons. The size and shape of the receptive fields were determined as a function of spike rate and first spike latency and showed differences for the two analysis methods used. Spatial diameters ranged from 2 to 36 mm (spike rate) and from 2.45 to 14.12 mm (first spike latency). Some of the receptive fields were simple consisting only of one uniform centre, whereas most receptive fields showed a complex and antagonistic centre-surround organisation. Several units had a very complex structure with multiple centres and surrounding-areas. While receptive field size did not correlate with peripheral receptor location, the complexity of the receptive fields increased from rostral to caudal along the fish's body.

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

Sensory neurons encode natural stimuli by changes in firing rate or by generating specific firing patterns, such as bursts. Many neural computations rely on the fact that neurons can be tuned to specific stimulus frequencies. It is thus important to understand the mechanisms underlying frequency tuning. In the electrosensory system of the weakly electric fish, Apteronotus leptorhynchus, the primary processing of behaviourally relevant sensory signals occurs in pyramidal neurons of the electrosensory lateral line lobe (ELL). These cells encode low frequency prey stimuli with bursts of spikes and high frequency communication signals with single spikes. We describe here how bursting in pyramidal neurons can be regulated by intrinsic conductances in a cell subtype specific fashion across the sensory maps found within the ELL, thereby regulating their frequency tuning. Further, the neuromodulatory regulation of such conductances within individual cells and the consequences to frequency tuning are highlighted. Such alterations in the tuning of the pyramidal neurons may allow weakly electric fish to preferentially select for certain stimuli under various behaviourally relevant circumstances.

In vitro studies of closed-loop feedback and electrosensory processing in Apteronotus leptorhynchus

Electrosensory systems comprise extensive feedback pathways. It is also well known that these pathways exhibit synaptic plasticity on a wide-range of time scales. Recent in vitro brain slice studies have characterized synaptic plasticity in the two main feedback pathways to the electrosensory lateral line lobe (ELL), a primary electrosensory nucleus in Apteronotus leptorhynchus. Currently-used slice preparations, involving networks in open-loop conditions, allow feedback inputs to be studied in isolation, a critical step in determining their synaptic properties. However, to fully understand electrosensory processing, we must understand how dynamic feedback modulates neuronal responses under closed-loop conditions. To bridge the gap between current in vitro approaches and more complex in vivo work, we present two new in vitro approaches for studying the roles of closed-loop feedback in electrosensory processing. The first involves a hybrid-network approach using dynamic clamp, and the second involves a new slice preparation that preserves one of the feedback pathways to ELL in a closed-loop condition.

Design principles of sensory processing in cerebellum-like structures

Cerebellum-like structures are compared for two sensory systems: electrosensory and auditory. The electrosensory lateral line lobe of mormyrid electric fish is reviewed and the neural representation of electrosensory objects in this structure is modeled and discussed. The dorsal cochlear nucleus in the auditory brainstem of mammals is reviewed and new data are presented that characterize the responses of neurons in this structure in the mouse. Similarities between the electrosensory and auditory cerebellum-like structures are shown, in particular adaptive processes that may reduce responses to predictable stimuli. We suggest that the differences in the types of sensory objects may drive the differences in the anatomical and physiological characteristics of these two cerebellum-like structures.

Intrinsic Frequency Tuning in ELL Pyramidal Cells Varies Across Electrosensory Maps

The tuning of neuronal responsiveness to specific stimulus frequencies is an important computation across many sensory modalities. The weakly electric fish Apteronotus leptorhynchus detects amplitude modulations of a self-generated quasi-sinusoidal electric organ discharge to sense its environment. These fish have to parse a complicated electrosensory environment with a wide range of possible frequency content. One solution has been to create multiple representations of the sensory input across distinct maps in the electrosensory lateral line lobe (ELL) that participate in distinct behavioral functions. E- and I-type pyramidal cells in the ELL that process sensory input further exhibit a preferred range of stimulus frequencies in relation to the different behaviors and sensory maps. We tested the hypothesis that variations in the intrinsic spiking mechanism of E- and I-type pyramidal cells contribute to map-specific frequency tuning. We find that E-cells exhibit a systematic change in their intrinsic spike characteristics and frequency tuning across sensory maps, whereas I-cells are constant in both spike characteristics and frequency tuning. As frequency tuning becomes more high-pass in E-cells, the refractory variables of spike half-width and afterhyperpolarization magnitude increase, spike threshold increases, adaptation becomes faster, and the gain of the spiking response decreases. These findings indicate that frequency tuning across sensory maps in the ELL is supported by differences in the intrinsic spike characteristics of pyramidal cells, revealing a link between cellular biophysical properties and signal processing in sensory maps with defined behavioral roles.

Differential distribution of SK channel subtypes in the brain of the weakly electric fish Apteronotus leptorhynchus

Calcium signals in vertebrate neurons can induce hyperpolarizing membrane responses through the activation of Ca(2+)-activated potassium channels. Of these, small conductance (SK) channels regulate neuronal responses through the generation of the medium after-hyperpolarization (mAHP). We have previously shown that an SK channel (AptSK2) contributes to signal processing in the electrosensory system of Apteronotus leptorhynchus. It was shown that for pyramidal neurons in the electrosensory lateral line lobe (ELL), AptSK2 expression selectively decreases responses to low-frequency signals. The localization of all the SK subunits throughout the brain of Apteronotus then became of substantial interest. We have now cloned two additional SK channel subunits from Apteronotus and determined the expression patterns of all three AptSK subunits throughout the brain. In situ hybridization experiments have revealed that, as in mammalian systems, the AptSK1 and 2 channels showed a partially overlapping expression pattern, whereas the AptSK3 channel was expressed in different brain areas. The AptSK1 and 2 channels were the primary subunits found in the major electrosensory processing areas. Immunohistochemistry further revealed distinct compartmentalization of the AptSK1 and 2 channels in the ELL. AptSK1 was localized to the apical dendrites of pyramidal neurons, whereas AptSK2 channels are primarily somatic. The distinct expression patterns of all three AptSK channels may reflect subtype-specific contributions to neuronal function, and the high homology between subtypes from a number of species suggests that the functional roles for each channel subtype are conserved from early vertebrate evolution.