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.

15In mammals, the localization of distinct landmarks is performed by hippocampal neurons 16 that sparsely encode an animal's location relative to surrounding objects. Similarly, the dorsal 17 lateral pallium (DL) is essential for spatial learning in teleost fish. The DL of weakly electric 18 gymnotiform fish receives sensory inputs from the preglomerular nucleus (PG), which has been 19 hypothesized to encode the temporal sequence of electrosensory or visual landmark/food 20 encounters. Here, we show that DL neurons have a hyperpolarized resting membrane potential 21 combined with a high and dynamic spike threshold that increases following each spike. Current-22 evoked spikes in DL cells are followed by a strong small-conductance calcium-activated 23 potassium channel (SK) mediated after-hyperpolarizing potential (AHP). Together, these 24 properties prevent high frequency and continuous spiking. The resulting sparseness of discharge 25 and dynamic threshold suggest that DL neurons meet theoretical requirements for generating 26 spatial memory engrams by decoding the landmark/

The localization of distinct landmarks plays a crucial role in encoding new spatial memories. In mammals, this function is performed by hippocampal neurons that sparsely encode an animal’s location relative to surrounding objects. Similarly, the dorsolateral pallium (DL) is essential for spatial learning in teleost fish. The DL of weakly electric gymnotiform fish receives both electrosensory and visual input from the preglomerular nucleus (PG), which has been hypothesized to encode the temporal sequence of electrosensory or visual landmark/food encounters. Here, we show that DL neurons in the Apteronotid fish and in the Carassius auratus (goldfish) have a hyperpolarized resting membrane potential (RMP) combined with a high and dynamic spike threshold that increases following each spike. Current-evoked spikes in DL cells are followed by a strong small-conductance calcium-activated potassium channel (SK)-mediated after-hyperpolarizing potential (AHP). Together, these properties prevent high frequency and continuous spiking. The resulting sparseness of discharge and dynamic threshold suggest that DL neurons meet theoretical requirements for generating spatial memory engrams by decoding the landmark/food encounter sequences encoded by PG neurons. Thus, DL neurons in teleost fish may provide a promising, simple system to study the core cell and network mechanisms underlying spatial memory.

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Hilar mossy cells (hMCs) are glutamatergic neurons in the dentate gyrus (DG) that receive inputs primarily from DG granule cells (GCs), CA3 pyramidal cells and local inhibitory interneurons. The hMCs then provide direct excitatory and disynaptic inhibitory feedback input to GCs. Behavioral and in vivo single unit recording experiments have implicated hMCs in pattern separation as well as is in spatial navigation and learning. It has, however, been difficult to mechanistically link the in vivo physiological behavior of hMCs with their intrinsic excitability properties that convert their synaptic inputs into spiking output. Here, we carried out electrophysiological recordings from the main cell types in the DG and found that hMCs displayed a highly adaptive threshold acting over a remarkably protracted time-scale. The hMC spike threshold increased linearly with increasing current stimulation and saturated at high current intensities. This threshold also increased in response to spiking and this effect also decayed over a long timescale, allowing for activity-dependent summation that limited hMC firing rates. This mechanism operates in parallel with a prominent medium after-hyperpolarizing potential (AHP) generated by the small conductance K+ channel. Based on experimentally derived parameters, we developed a phenomenological exponential integrate-and-fire model that closely mimics the hMC adaptive threshold. This lightweight model is amenable to its incorporation into large network models of the DG that will be conducive to deepen our understanding of the neural bases of pattern separation, spatial learning and navigation in the hippocampus.