TY - JOUR
T1 - Connectomics of the Octopus vulgaris vertical lobe provides insight into conserved and novel principles of a memory acquisition network
AU - Bidel, Flavie
AU - Meirovitch, Yaron
AU - Schalek, Richard Lee
AU - Lu, Xiaotang
AU - Pavarino, Elisa Catherine
AU - Yang, Fuming
AU - Peleg, Adi
AU - Wu, Yuelong
AU - Shomrat, Tal
AU - Berger, Daniel Raimund
AU - Shaked, Adi
AU - Lichtman, Jeff William
AU - Hochner, Binyamin
N1 - Publisher Copyright:
© 2023, Bidel, Meirovitch et al.
PY - 2023/7/6
Y1 - 2023/7/6
N2 - Here, we present the first analysis of the connectome of a small volume of the Octopus vulgaris vertical lobe (VL), a brain structure mediating the acquisition of long-term memory in this behaviorally advanced mollusk. Serial section electron microscopy revealed new types of interneurons, cellular components of extensive modulatory systems, and multiple synaptic motifs. The sensory input to the VL is conveyed via~1.8 × 106 axons that sparsely innervate two parallel and interconnected feedforward networks formed by the two types of amacrine interneurons (AM), simple AMs (SAMs) and complex AMs (CAMs). SAMs make up 89.3% of the~25 × 106VL cells, each receiving a synaptic input from only a single input neuron on its non-bifurcating primary neurite, suggesting that each input neuron is represented in only~12 ± 3.4SAMs. This synaptic site is likely a 'memory site' as it is endowed with LTP. The CAMs, a newly described AM type, comprise 1.6% of the VL cells. Their bifurcating neurites integrate multiple inputs from the input axons and SAMs. While the SAM network appears to feedforward sparse 'memorizable' sensory representations to the VL output layer, the CAMs appear to monitor global activity and feedforward a balancing inhibition for 'sharpening' the stimulus-specific VL output. While sharing morphological and wiring features with circuits supporting associative learning in other animals, the VL has evolved a unique circuit that enables associative learning based on feedforward information flow.
AB - Here, we present the first analysis of the connectome of a small volume of the Octopus vulgaris vertical lobe (VL), a brain structure mediating the acquisition of long-term memory in this behaviorally advanced mollusk. Serial section electron microscopy revealed new types of interneurons, cellular components of extensive modulatory systems, and multiple synaptic motifs. The sensory input to the VL is conveyed via~1.8 × 106 axons that sparsely innervate two parallel and interconnected feedforward networks formed by the two types of amacrine interneurons (AM), simple AMs (SAMs) and complex AMs (CAMs). SAMs make up 89.3% of the~25 × 106VL cells, each receiving a synaptic input from only a single input neuron on its non-bifurcating primary neurite, suggesting that each input neuron is represented in only~12 ± 3.4SAMs. This synaptic site is likely a 'memory site' as it is endowed with LTP. The CAMs, a newly described AM type, comprise 1.6% of the VL cells. Their bifurcating neurites integrate multiple inputs from the input axons and SAMs. While the SAM network appears to feedforward sparse 'memorizable' sensory representations to the VL output layer, the CAMs appear to monitor global activity and feedforward a balancing inhibition for 'sharpening' the stimulus-specific VL output. While sharing morphological and wiring features with circuits supporting associative learning in other animals, the VL has evolved a unique circuit that enables associative learning based on feedforward information flow.
KW - caphalopods
KW - connectome
KW - feedforward
KW - invertebrate
KW - learning
KW - memory
KW - neuroscience
KW - octopus
UR - http://www.scopus.com/inward/record.url?scp=85164253883&partnerID=8YFLogxK
U2 - 10.7554/eLife.84257
DO - 10.7554/eLife.84257
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C2 - 37410519
AN - SCOPUS:85164253883
SN - 2050-084X
VL - 12
JO - eLife
JF - eLife
ER -