Abstract
There is an ongoing debate on the evolutionary origin of the episodic memory function of the hippocampus. A widely accepted hypothesis claims that the hippocampus first evolved as a dedicated system for spatial navigation in ancestral vertebrates, being transformed later in phylogeny to support a broader role in episodic memory with the emergence of mammals. On the contrary, an alternative hypothesis holds that the hippocampus of ancestral vertebrates originally encoded both the spatial and temporal dimensions of relational memories since its evolutionary appearance, thus suggesting that the episodic-like memory function of the hippocampus could be the primitive condition in vertebrate forebrain evolution. The present experiment was aimed at scrutinizing these opposing hypotheses by investigating whether the hippocampal pallium of teleost fish, a vertebrate group that shares with mammals a common ancestor that lived about 400 Mya, is, like the hippocampus of mammals, essential to associate time-discontiguous events. Thus, goldfish with lesions in the ventral part of the dorsolateral pallium (Dlv), a telencephalic region considered homologous to the hippocampal pallium of land vertebrates, were trained in trace versus delay eyeblink-like classical conditioning, two learning procedures that differ only in the temporal relationships between the stimuli to be associated in memory. The results showed that hippocampal pallium lesion in goldfish severely impairs trace conditioning, but spares delay conditioning. This finding challenges the idea that navigation preceded relational memory in evolutionary appearance and suggests the possibility that a relational memory function that associates the experienced events in both the spatial and temporal dimensions could be a primitive feature of the hippocampus that pre-existed in the common ancestor of vertebrates.
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Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
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Acknowledgements
This study was supported by grants PID2020-117359GB-I00 from the Spanish Government and US-1264766 from Junta de Andalucía and European Union FEDER. We are grateful to Drs. Cristina Broglio and Emilio Durán for their helpful comments on this paper, and Eduardo Cueto for technical support.
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Ministerio de Economía, Industria y Competitividad, Gobierno de España, PID2020-117359 GB-I00, Cosme Salas, Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía, US-1264766, Cosme Salas
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AG, CS, and FR: conceived and designed the study; BR, AG, CS and FR: conducted the experiments; BR, AG, and FO: analyzed the data; CS, FR, and AG: wrote the manuscript; CS and FR: obtained funding and supervised the study.
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Gómez, A., Rodríguez-Expósito, B., Ocaña, F.M. et al. Trace classical conditioning impairment after lesion of the lateral part of the goldfish telencephalic pallium suggests a long ancestry of the episodic memory function of the vertebrate hippocampus. Brain Struct Funct 227, 2879–2890 (2022). https://doi.org/10.1007/s00429-022-02553-3
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DOI: https://doi.org/10.1007/s00429-022-02553-3