TY - JOUR
T1 - The Rhesus monkey Hippocampus critically contributes to scene memory retrieval, but not new learning
AU - Froudist-Walsh, Sean
AU - Browning, Philip G.F.
AU - Croxson, Paula L.
AU - Murphy, Kathy L.
AU - Shamy, Jul Lea
AU - Veuthey, Tess L.
AU - Wilson, Charles R.E.
AU - Baxter, Mark G.
N1 - Funding Information:
This work was supported by a Wellcome Trust Senior Research Fellowship 071291, Friedman Brain Institute at the Icahn School of Medicine at Mount Sinai. We thank Peter Sergo for help testing the monkeys; James Young, Charles Adapoe, Frank Macaluso, Ronald Primm, Ignacio Medel, Pedro Hernandez, and Lazar Fleysher for help with MRI scans; Bill Janssen for help with perfusions; Richard Saunders for advice on the hippocampal neurosurgical approach; and David Gaffan for advice on experimental design.
Publisher Copyright:
© 2018 the authors.
PY - 2018/9/5
Y1 - 2018/9/5
N2 - Humans can recall a large number of memories years after the initial events. Patients with amnesia often have lesions to the hippocampus, but human lesions are imprecise, making it difficult to identify the anatomy underlying memory impairments. Rodent studies enable great precision in hippocampal manipulations, but not investigation of many interleaved memories. 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 temporally graded or ungraded amnesia, which could be a consequence of differences between rodent and human studies. In the current study, rhesus monkeys of both sexes received either bilateral neurotoxic hippocampal lesions or remained unoperated controls and were tested on recognition and new learning of visual object-in-place scenes. Monkeys with hippocampal lesions were significantly impaired 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 new scenes. Thus, the hippocampus, like other cortical regions, may be engaged in the acquisition and storage of new memories, but the role of the damaged hippocampus can be taken over by spared hippocampal tissue or extra-hippocampal 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.
AB - Humans can recall a large number of memories years after the initial events. Patients with amnesia often have lesions to the hippocampus, but human lesions are imprecise, making it difficult to identify the anatomy underlying memory impairments. Rodent studies enable great precision in hippocampal manipulations, but not investigation of many interleaved memories. 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 temporally graded or ungraded amnesia, which could be a consequence of differences between rodent and human studies. In the current study, rhesus monkeys of both sexes received either bilateral neurotoxic hippocampal lesions or remained unoperated controls and were tested on recognition and new learning of visual object-in-place scenes. Monkeys with hippocampal lesions were significantly impaired 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 new scenes. Thus, the hippocampus, like other cortical regions, may be engaged in the acquisition and storage of new memories, but the role of the damaged hippocampus can be taken over by spared hippocampal tissue or extra-hippocampal 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.
KW - Anterograde amnesia
KW - Episodic
KW - Macaque
KW - Memory
KW - Retrograde amnesia
KW - Rhesus
UR - http://www.scopus.com/inward/record.url?scp=85053085848&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.0832-18.2018
DO - 10.1523/JNEUROSCI.0832-18.2018
M3 - Article
C2 - 30049888
AN - SCOPUS:85053085848
SN - 0270-6474
VL - 38
SP - 7800
EP - 7808
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 36
ER -