Virtual Environmental Enrichment through Video Games Improves Hippocampal-Associated Memory

The positive effects of environmental enrichment and their neural bases have been studied extensively in the rodent (van Praag et al., 2000). For example, simply modifying an animal's living environment to promote sensory stimulation can lead to (but is not limited to) enhancements in hippocampal cognition and neuroplasticity and can alleviate hippocampal cognitive deficits associated with neurodegenerative diseases and aging. We are interested in whether these manipulations that successfully enhance cognition (or mitigate cognitive decline) have similar influences on humans. Although there are many “enriching” aspects to daily life, we are constantly adapting to new experiences and situations within our own environment on a daily basis. Here, we hypothesize that the exploration of the vast and visually stimulating virtual environments within video games is a human correlate of environmental enrichment. We show that video gamers who specifically favor complex 3D video games performed better on a demanding recognition memory task that assesses participants' ability to discriminate highly similar lure items from repeated items. In addition, after 2 weeks of training on the 3D video game Super Mario 3D World, naive video gamers showed improved mnemonic discrimination ability and improvements on a virtual water maze task. Two control conditions (passive and training in a 2D game, Angry Birds), showed no such improvements. Furthermore, individual performance in both hippocampal-associated behaviors correlated with performance in Super Mario but not Angry Birds, suggesting that how individuals explored the virtual environment may influence hippocampal behavior. SIGNIFICANCE STATEMENT The hippocampus has long been associated with episodic memory and is commonly thought to rely on neuroplasticity to adapt to the ever-changing environment. In animals, it is well understood that exposing animals to a more stimulating environment, known as environmental enrichment, can stimulate neuroplasticity and improve hippocampal function and performance on hippocampally mediated memory tasks. Here, we suggest that the exploration of vast and visually stimulating environments within modern-day video games can act as a human correlate of environmental enrichment. Training naive video gamers in a rich 3D, but not 2D, video game, resulted in a significant improvement in hippocampus-associated cognition using several behavioral measures. Our results suggest that modern day video games may provide meaningful stimulation to the human hippocampus.

[1]  C Brock Kirwan,et al.  Overcoming interference: an fMRI investigation of pattern separation in the medial temporal lobe. , 2007, Learning & memory.

[2]  Gerd Kempermann,et al.  Additive Effects of Physical Exercise and Environmental Enrichment on Adult Hippocampal Neurogenesis in Mice , 2009, Front. Neurogenesis.

[3]  R. Morris Developments of a water-maze procedure for studying spatial learning in the rat , 1984, Journal of Neuroscience Methods.

[4]  Wei Deng,et al.  Enrichment rescues contextual discrimination deficit associated with immediate shock , 2015, Hippocampus.

[5]  C. Stark,et al.  Pattern Separation in the Human Hippocampal CA3 and Dentate Gyrus , 2008, Science.

[6]  Chunmei Zhao,et al.  Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers , 2014, The Journal of comparative neurology.

[7]  F. Gage,et al.  More hippocampal neurons in adult mice living in an enriched environment , 1997, Nature.

[8]  C. S. Green,et al.  Enumeration versus multiple object tracking: the case of action video game players , 2006, Cognition.

[9]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P. Frankland,et al.  Age‐dependent effects of hippocampal neurogenesis suppression on spatial learning , 2013, Hippocampus.

[11]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[12]  Mareike Kritzler,et al.  Emergence of Individuality in Genetically Identical Mice , 2013, Science.

[13]  F. Gage,et al.  Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus , 1999, Nature Neuroscience.

[14]  Á. Kelly,et al.  Short‐term environmental enrichment, in the absence of exercise, improves memory, and increases NGF concentration, early neuronal survival, and synaptogenesis in the dentate gyrus in a time‐dependent manner , 2013, Hippocampus.

[15]  M. Häusser,et al.  Cellular mechanisms of spatial navigation in the medial entorhinal cortex , 2013, Nature Neuroscience.

[16]  B. Christie,et al.  Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways , 2006, Hippocampus.

[17]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[18]  C. Stark,et al.  Pattern separation in the hippocampus , 2011, Trends in Neurosciences.

[19]  R. Morris Spatial Localization Does Not Require the Presence of Local Cues , 1981 .

[20]  F. Gage,et al.  Neurogenesis in the adult human hippocampus , 1998, Nature Medicine.

[21]  F. Gage,et al.  Spine morphogenesis in newborn granule cells is differentially regulated in the outer and middle molecular layers , 2015, The Journal of comparative neurology.

[22]  A. Fenton,et al.  Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation , 2011, Nature.

[23]  R. Skelton,et al.  Spatial deficits in a virtual water maze in amnesic participants with hippocampal damage , 2009, Hippocampus.

[24]  P. Rodríguez Human navigation that requires calculating heading vectors recruits parietal cortex in a virtual and visually sparse water maze task in fMRI. , 2010, Behavioral neuroscience.

[25]  Elizabeth R. Chrastil,et al.  Active and passive contributions to spatial learning , 2011, Psychonomic Bulletin & Review.

[26]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[27]  Fred H. Gage,et al.  Exercise Enhances Learning and Hippocampal Neurogenesis in Aged Mice , 2005, The Journal of Neuroscience.

[28]  Shauna M. Stark,et al.  A task to assess behavioral pattern separation (BPS) in humans: Data from healthy aging and mild cognitive impairment , 2013, Neuropsychologia.

[29]  Lisa M. Saksida,et al.  Running enhances spatial pattern separation in mice , 2010, Proceedings of the National Academy of Sciences.

[30]  Hagen B. Huttner,et al.  Dynamics of Hippocampal Neurogenesis in Adult Humans , 2013, Cell.

[31]  N. Fortin,et al.  Critical Role of the Hippocampus in Memory for Elapsed Time , 2013, The Journal of Neuroscience.

[32]  N. Burgess Spatial Cognition and the Brain , 2008, Annals of the New York Academy of Sciences.

[33]  Anders Petersen,et al.  Intensive video gaming improves encoding speed to visual short-term memory in young male adults. , 2013, Acta psychologica.

[34]  D. Tank,et al.  Intracellular dynamics of hippocampal place cells during virtual navigation , 2009, Nature.

[35]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[36]  Lynette J. Tippett,et al.  The virtual brain: 30 years of video-game play and cognitive abilities , 2013, Front. Psychol..

[37]  Arne D. Ekstrom,et al.  Cellular networks underlying human spatial navigation , 2003, Nature.

[38]  P. Dudchenko The hippocampus as a cognitive map , 2010 .

[39]  Mirjana Maletic-Savatic,et al.  Comment on "Magnetic Resonance Spectroscopy Identifies Neural Progenitor Cells in the Live Human Brain" , 2008, Science.

[40]  Shauna M. Stark,et al.  Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high-resolution fMRI and variable mnemonic similarity. , 2010, Learning & memory.

[41]  S. Kühn,et al.  Playing Super Mario induces structural brain plasticity: gray matter changes resulting from training with a commercial video game , 2014, Molecular Psychiatry.

[42]  C. Stark,et al.  Mnemonic discrimination relates to perforant path integrity: An ultra-high resolution diffusion tensor imaging study , 2016, Neurobiology of Learning and Memory.

[43]  G. Deuschl,et al.  Focal Lesions of Human Hippocampal CA1 Neurons in Transient Global Amnesia Impair Place Memory , 2010, Science.

[44]  Naomi J. Goodrich-Hunsaker,et al.  Pattern separation deficits following damage to the hippocampus , 2012, Neuropsychologia.

[45]  L. Saksida,et al.  A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation , 2009, Science.

[46]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

[47]  Larry R Squire,et al.  Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. , 2009, Learning & memory.

[48]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[49]  Hugo J Spiers,et al.  Talent in the taxi: a model system for exploring expertise , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  Greg L. West,et al.  Habitual action video game playing is associated with caudate nucleus-dependent navigational strategies , 2015, Proceedings of the Royal Society B: Biological Sciences.