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The rhesus monkey hippocampus critically contributes to scene memory retrieval, but not new learning

View ORCID ProfileSean Froudist-Walsh, Philip G. F. Browning, Paula L. Croxson, Kathy L. Murphy, Jul Lea Shamy, Tess L. Veuthey, Charles R. E. Wilson, Mark G. Baxter
doi: https://doi.org/10.1101/288407
Sean Froudist-Walsh
1Glickenhaus Laboratory of Neuropsychology, Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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  • ORCID record for Sean Froudist-Walsh
Philip G. F. Browning
1Glickenhaus Laboratory of Neuropsychology, Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Paula L. Croxson
1Glickenhaus Laboratory of Neuropsychology, Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Kathy L. Murphy
1Glickenhaus Laboratory of Neuropsychology, Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Jul Lea Shamy
1Glickenhaus Laboratory of Neuropsychology, Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Tess L. Veuthey
1Glickenhaus Laboratory of Neuropsychology, Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Charles R. E. Wilson
2Univ Lyon, Université Claude Bernard Lyon 1, Inserm, Stem Cell and Brain Research Institute U1208, 69500 Bron, France
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Mark G. Baxter
1Glickenhaus Laboratory of Neuropsychology, Department of Neuroscience and Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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  • For correspondence: mark.baxter@mssm.edu
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Abstract

Humans can recall a large number of memories years after the events that triggered them. Early studies of humans with amnesia led to the hippocampus being viewed as the critical structure for episodic memory, but human lesions are imprecise, making it difficult to identify the anatomical structures underlying memory impairments. Rodent studies enable great temporal and anatomical precision in hippocampal manipulations, but not investigation of the rich assortment of interleaved memories that occurs in humans. Thus it is not known how lesions restricted to the hippocampus affect the retrieval of multiple sequentially encoded memories. Furthermore, disagreement exists as to whether hippocampal inactivations lead to a temporally graded, or ungraded amnesia, which could be a consequence of different types hippocampal disruption observed in rodent and human studies. In the current study, four rhesus monkeys received bilateral neurotoxic lesions of the hippocampus, and were compared to thirteen unoperated controls on recognition and new learning of visual object-in-place scenes. Monkeys with hippocampal lesions were significantly impaired compared to controls at remembering scenes that were encoded before the lesion. We did not observe any temporal gradient effect of the lesion on memory recognition, with recent and remote memories being equally affected by the lesion. Monkeys with hippocampal lesions showed no deficits in learning and later recognising new scenes. Thus, the hippocampus, like other cortical regions, may be engaged in the acquisition and storage of new memories, but its role can be taken over by spared regions following a lesion. These findings illustrate the utility of experimental paradigms for studying retrograde and anterograde amnesia that make use of the capacity of nonhuman primates to rapidly acquire many distinct visual memories.

Footnotes

  • Grant support: Wellcome Trust Senior Research Fellowship 071291, Friedman Brain Institute at the Icahn School of Medicine at Mount Sinai

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted March 24, 2018.
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The rhesus monkey hippocampus critically contributes to scene memory retrieval, but not new learning
Sean Froudist-Walsh, Philip G. F. Browning, Paula L. Croxson, Kathy L. Murphy, Jul Lea Shamy, Tess L. Veuthey, Charles R. E. Wilson, Mark G. Baxter
bioRxiv 288407; doi: https://doi.org/10.1101/288407
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The rhesus monkey hippocampus critically contributes to scene memory retrieval, but not new learning
Sean Froudist-Walsh, Philip G. F. Browning, Paula L. Croxson, Kathy L. Murphy, Jul Lea Shamy, Tess L. Veuthey, Charles R. E. Wilson, Mark G. Baxter
bioRxiv 288407; doi: https://doi.org/10.1101/288407

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