Evidence for an Evolutionarily Conserved Memory Coding Scheme in the Mammalian Hippocampus.
Decades of research identify the hippocampal formation as central to memory storage and recall. Events are stored via distributed population codes, the parameters of which (e.g., sparsity and overlap) determine both storage capacity and fidelity. However, it remains unclear whether the parameters governing information storage are similar between species. Because episodic memories are rooted in the space in which they are experienced, the hippocampal response to navigation is often used as a proxy to study memory. Critically, recent studies in rodents that mimic the conditions typical of navigation studies in humans and nonhuman primates (i.e., virtual reality) show that reduced sensory input alters hippocampal representations of space. The goal of this study was to quantify this effect and determine whether there are commonalities in information storage across species. Using functional molecular imaging, we observe that navigation in virtual environments elicits activity in fewer CA1 neurons relative to real-world conditions. Conversely, comparable neuronal activity is observed in hippocampus region CA3 and the dentate gyrus under both conditions. Surprisingly, we also find evidence that the absolute number of neurons used to represent an experience is relatively stable between nonhuman primates and rodents. We propose that this convergence reflects an optimal ensemble size for episodic memories.SIGNIFICANCE STATEMENTOne primary factor constraining memory capacity is the sparsity of the engram, the proportion of neurons that encode a single experience. Investigating sparsity in humans is hampered by the lack of single-cell resolution and differences in behavioral protocols. Sparsity can be quantified in freely moving rodents, but extrapolating these data to humans assumes that information storage is comparable across species and is robust to restraint-induced reduction in sensory input. Here, we test these assumptions and show that species differences in brain size build memory capacity without altering the structure of the data being stored. Furthermore, sparsity in most of the hippocampus is resilient to reduced sensory information. This information is vital to integrating animal data with human imaging navigation studies.
Evelyn F. McKnight Brain Institute.|Division of Neural Systems, Memory and Aging, and.
Alexander
A
Thome
Evelyn F. McKnight Brain Institute.|Department of Psychology, Wilfrid Laurier University, Waterloo, Ontario N2L 3C5, Canada.
Diano F
0000-0001-8422-8536
DF
Marrone
Department of Psychology, The City College of New York, New York, New York 10031.
Timothy M
0000-0001-6125-0044
TM
Ellmore
Evelyn F. McKnight Brain Institute.|Division of Neural Systems, Memory and Aging, and.
Monica K
0000-0002-0446-8992
MK
Chawla
Evelyn F. McKnight Brain Institute.|Division of Neural Systems, Memory and Aging, and.
Peter
0000-0001-9904-465X
P
Lipa
Maestría en Neruometabolismo, Fac. de Medicina, Universidad Autónoma de Queretaro, 76010 Santiago de Queretaro, QRO, Mexico.|Instituto de Investigación Médica Mercedes y Martín Ferreyra, 5016 Córdoba, Argentina.
Victor
0000-0001-9670-8692
V
Ramirez-Amaya
Department of Psychiatry and Behavioral Sciences, Duke University, Durham, North Carolina 27708.
Sarah H
SH
Lisanby
Department of Neuroscience, Canadian Centre for Behavioural Neuroscience, The University of Lethbridge, Lethbridge, Alberta T1K 6T5, Canada, and.|Center for the Neurobiology of Learning and Memory, University of California, Irvine, Irvine, California 92697.
Bruce L
BL
McNaughton
Evelyn F. McKnight Brain Institute, carol@nsma.arizona.edu.|Division of Neural Systems, Memory and Aging, and.|Department of Psychology, Neurology and Neuroscience, University of Arizona, Tucson, Arizona 85724.
Carol A
0000-0001-8122-9007
CA
Barnes
D000818:Animals; D005075:Biological Evolution; D019317:Evidence-Based Medicine; D006624:Hippocampus / Q000502:physiology*; D008253:Macaca mulatta; D008297:Male; D061212:Memory, Episodic; D009415:Nerve Net / Q000502:physiology*; D009949:Orientation / Q000502:physiology*; D013045:Species Specificity
neural coding; neuroethology; primate; rodent; spatial cognition; virtual reality