One important characteristic of sensory input is frequency, with sensory neurons often tuned to narrow stimulus frequency ranges. Although vital for many neural computations, the cellular basis of such frequency tuning remains mostly unknown. In the electrosensory system of Apteronotus leptorhynchus, the primary processing of important environmental and communication signals occurs in pyramidal neurons of the electrosensory lateral line lobe. Spike trains transmitted by these cells can encode low-frequency prey stimuli with bursts of spikes and high-frequency communication signals with single spikes. Here, we demonstrate that the selective expression of SK2 channels in a subset of pyramidal neurons reduces their response to low-frequency stimuli by opposing their burst responses. Apamin block of the SK2 current in this subset of cells induced bursting and increased their response to low-frequency inputs. SK channel expression thus provides an intrinsic mechanism that predisposes a neuron to respond to higher frequencies and thus specific, behaviorally relevant stimuli.

The present article examines the anatomical organization of the dorsal telencephalon of two gymnotiform fish: Gymnotus sp. and Apteronotus leptorhynchus. These electric fish use elaborate electrical displays for agonistic and sexual communication. Our study emphasizes mainly pallial divisions: dorsolateral (DL), dorsodorsal (DD), and dorsocentral (DC), previously implicated in social learning dependent on electric signals. We found that the pallial cytoarchitectonics of gymnotiformes are similar to those reported for the commonly studied goldfish, except that DC is larger and better differentiated in gymnotiformes. We identified a new telencephalic region (Dx), located between DL and DC, and describe the morphological and some biochemical properties of its neurons. Most neurons in DL, DD, and DC are glutamatergic with spiny dendrites. However, the size of these cells as well as the orientation and extent of their dendrites vary systematically across these regions. In addition, both DD and DL contained numerous small GABAergic interneurons as well as well-developed GABAergic plexuses. One important and novel observation is that the dendrites of the spiny neurons within all three regions remain confined to their respective territories. We confirm that DL and DC express very high levels of NMDA receptor subunits as well as CaMKIIα, a key downstream effector of this receptor. In contrast, this enzyme is nearly absent in DD, while NMDA receptors are robustly expressed, suggesting different rules for synaptic plasticity across these regions. Remarkably, GABAergic pallial neurons do not express CaMKIIα, in agreement with previously reported results in the cortex of rats.

For optimal sensory processing, neural circuits must extract novel, unpredictable signals from the redundant sensory input in which they are embedded, but the detailed cellular and network mechanisms that implement such selective cancellation are presently unknown. Using a combination of modeling and experiment, we characterize in detail a cerebellar circuit in weakly electric fish, showing how it can carry out this computation. We use a model incorporating the wide range of experimentally estimated parallel fiber feedback delays and a burst-induced LTD rulederivedfrominvitroexperimentstoexplaintheprecisecancellationofredundantsignalsobservedinvivo.Ourmodeldemonstrateshowthe backpropagation-dependent burst dynamics adjusts the temporal pairing width of the plasticity mechanism to precisely match the frequency of the redundant signal. The model also makes the prediction that this cerebellar feedback pathway must be composed of frequency-tuned channels; this prediction is subsequently verified in vivo, highlighting a novel and general capability of cerebellar circuitry.

Teleost fish are capable of complex behaviors, including social and spatial learning; lesion studies show that these abilities require dorsal telencephalon (pallium). The teleost telencephalon has subpallial and pallial components. The subpallium is well described and highly conserved. In contrast, the teleost pallium is not well understood and its relation to that of other vertebrates remains controversial. Here we analyze the connectivity of the subdivisions of dorsal pallium (DD) of an electric gymnotiform fish, Apteronotus leptorhynchus: superficial (DDs), intermediate (DDi) and magnocellular (DDmg) components. The major pathways are recursive: the dorsolateral pallium (DL) projects strongly to DDi, with lesser inputs to DDs and DDmg. DDi in turn projects strongly to DDmg, which then feeds back diffusely to DL. Our quantitative analysis of DDi connectivity demonstrates that it is a global recurrent network. In addition, we show that the DD subnuclei have complex reciprocal connections with subpallial regions. Specifically, both DDi and DDmg are reciprocally connected to pallial interneurons within the misnamed rostral entopeduncular nucleus (Er). Based on DD connectivity, we illustrate the close similarity, and possible homology, between hippocampal and DD/DL circuitry. We hypothesize that DD/DL circuitry can implement the same pattern separation and completion computations ascribed to the hippocampal dentate gyrus and CA3 fields. We further contend that the DL to DDi to DDmg to DL feedback loop makes the pattern separation/completion operations recursive. We discuss our results with respect to recent studies on fear avoidance conditioning in zebrafish and attention and spatial learning in a pulse gymnotiform fish. J. Comp. Neurol. 525:8-46, 2017. © 2016 Wiley Periodicals, Inc.

In the weakly electric gymnotiform fish, Apteronotus leptorhynchus, the dorsolateral pallium (DL) receives diencephalic inputs representing electrosensory input utilized for communication and navigation. Cell counts reveal that, similar to thalamocortical projections, many more cells are present in DL than in the diencephalic nucleus that provides it with sensory input. DL is implicated in learning and memory and considered homologous to medial and/or dorsal pallium. The gymnotiform DL has an apparently simple architecture with a random distribution of simple multipolar neurons. We used multiple neurotracer injections in order to study the microcircuitry of DL. Surprisingly, we demonstrated that the intrinsic connectivity of DL is highly organized. It consists of orthogonal laminar and vertical excitatory synaptic connections. The laminar synaptic connections are symmetric sparse, random, and drop off exponentially with distance; they parcellate DL into narrow (60 μm) overlapping cryptic layers. At distances greater than 100 μm, the laminar connections generate a strongly connected directed graph architecture within DL. The vertical connectivity suggests that DL is also organized into cryptic columns; these connections are highly asymmetric, with superficial DL cells preferentially projecting towards deeper cells. Our experimental analyses suggest that the overlapping cryptic columns have a width of 100 μm, in agreement with the minimal distance for strong connectivity. The architecture of DL and the expansive representation of its input, taken together with the strong expression of N-methyl-D-aspartate (NMDA) receptors by its cells, are consistent with theoretical ideas concerning the cortical computations of pattern separation and memory storage via bump attractors.