Differential effect of sleep deprivation on place cell representations, sleep architecture, and memory in young and old mice
Robin K. Yuan,
Matthew R. Lopez,
Manuel-Miguel Ramos-Alvarez,
Marc E. Normandin,
Arthur S. Thomas,
David S. Uygun,
Vanessa R. Cerda,
Amandine E. Grenier,
Matthew T. Wood,
Celia M. Gagliardi,
Herminio Guajardo,
Isabel A. Muzzio
Affiliations
Robin K. Yuan
Division of Sleep and Circadian Disorders, Departments of Medicine and Neurology, Brigham and Women’s Hospital, 221 Longwood Avenue, Boston, MA, USA; Division of Sleep Medicine, Harvard Medical School, 221 Longwood Avenue, Boston, MA, USA
Matthew R. Lopez
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA
Manuel-Miguel Ramos-Alvarez
University of Jaen, Psychology Department, Campus Las Lagunillas, Jaen 23071, Spain
Marc E. Normandin
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA
Arthur S. Thomas
Perelman School of Medicine, University of Pennsylvania, 3400 Civic Center Boulevard, Philadelphia, PA 19104, USA
David S. Uygun
VA Boston Healthcare System and Department of Psychiatry, Harvard Medical School, West Roxbury, MA 02132, USA
Vanessa R. Cerda
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA
Amandine E. Grenier
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA
Matthew T. Wood
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA
Celia M. Gagliardi
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA
Herminio Guajardo
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA
Isabel A. Muzzio
University of Texas at San Antonio, Department of Biology, One UTSA Circle, San Antonio, TX 78249, USA; Corresponding author
Summary: Poor sleep quality is associated with age-related cognitive decline, and whether reversal of these alterations is possible is unknown. In this study, we report how sleep deprivation (SD) affects hippocampal representations, sleep patterns, and memory in young and old mice. After training in a hippocampus-dependent object-place recognition (OPR) task, control animals sleep ad libitum, although experimental animals undergo 5 h of SD, followed by recovery sleep. Young controls and old SD mice exhibit successful OPR memory, whereas young SD and old control mice are impaired. Successful performance is associated with two cellular phenotypes: (1) “context” cells, which remain stable throughout training and testing, and (2) “object configuration” cells, which remap when objects are introduced to the context and during testing. Additionally, effective memory correlates with spindle counts during non-rapid eye movement (NREM)/rapid eye movement (REM) sigma transitions. These results suggest SD may serve to ameliorate age-related memory deficits and allow hippocampal representations to adapt to changing environments.
