Hippocampal-like circuitry in the pallium of an electric fish: Possible substrates for recursive pattern separation and completion.
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.
Department of Cellular and Molecular Medicine, University of Ottawa, Ontario, Canada.
S Benjamin
0000-0001-7768-3071
SB
Elliott
Department of Cellular and Molecular Medicine, University of Ottawa, Ontario, Canada.
Erik
E
Harvey-Girard
Department of Cellular and Molecular Medicine, University of Ottawa, Ontario, Canada.
Ana C C
AC
Giassi
Department of Cellular and Molecular Medicine, University of Ottawa, Ontario, Canada.|Center for Neural Dynamics, Brain and Mind Institute, University of Ottawa, Ontario, Canada.
Leonard
L
Maler
D000818:Animals; D054022:Cerebrum / Q000033:anatomy & histology* / Q000378:metabolism; D017630:Connexins / Q000235:genetics / Q000378:metabolism; D004555:Electric Fish / Q000033:anatomy & histology* / Q000235:genetics / Q000378:metabolism; D025461:Feedback, Physiological; D029941:Fish Proteins / Q000235:genetics / Q000378:metabolism; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D008959:Models, Neurological; D009434:Neural Pathways / Q000033:anatomy & histology / Q000378:metabolism; D056347:Neuroanatomical Tract-Tracing Techniques; D016415:Sequence Alignment; D017386:Sequence Homology, Amino Acid; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
D017630:Connexins; D029941:Fish Proteins; C100585:connexin 35 protein, vertebrate; D005680:gamma-Aminobutyric Acid
basal ganglia; cortex; dentate gyrus; electric fish; evolution; hippocampus; memory; pattern completion; pattern separation; telencephalon; teleost fish