Abstract
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 dorsal lateral 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 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.
Significance Statement To our knowledge, this is first study of the intrinsic physiology of teleost pallial (DL) neurons. Their biophysical properties demonstrate that DL neurons are sparse coders with a dynamic spike threshold leading us to suggest that they can transform time-stamped input into spatial location during navigation. The concept of local attractors (bumps) that potentially move ‘across’ local recurrent networks has been prominent in the neuroscience theory literature. We propose that the relatively simple and experimentally accessible DL of teleosts may be the best preparation to examine this idea experimentally and to investigate the properties of local (excitatory) recurrent networks whose cells are endowed with, e.g., slow spike threshold adaptation dynamics.
- Hippocampus-like
- Recurrent network
- Sparse coding
- Spike threshold adaptation
- Time cell
- Weakly electric fish
Footnotes
The authors declare no conflicting financial or non-financial interests.
This research was supported by the Canadian Institutes of Health Research - CIHR 153143 and by the Natural Sciences and Engineering Research Council - NSERC 04336 grant, both assigned to LM.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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