Seasonal hippocampal plasticity in food-storing birds

Both food-storing behaviour and the hippocampus change annually in food-storing birds. Food storing increases substantially in autumn and winter in chickadees and tits, jays and nutcrackers and nuthatches. The total size of the chickadee hippocampus increases in autumn and winter as does the rate of hippocampal neurogenesis. The hippocampus is necessary for accurate cache retrieval in food-storing birds and is much larger in food-storing birds than in non-storing passerines. It therefore seems probable that seasonal change in caching and seasonal change in the hippocampus are causally related. The peak in recruitment of new neurons into the hippocampus occurs before birds have completed food storing and cache retrieval for the year and may therefore be associated with spacing caches, encoding the spatial locations of caches, or creating a neuronal architecture involved in the recollection of cache sites. The factors controlling hippocampal plasticity in food-storing birds are not well understood. Photoperiodic manipulations that produce change in food-storing behaviour have no effect on either hippocampal size or neuronal recruitment. Available evidence suggests that changes in hippocampal size and neurogenesis may be a consequence of the behavioural and cognitive involvement of the hippocampus in storing and retrieving food.

[1]  O. Hogstad Svein Haftorn Contribution to the food biology of tits, especially about storing of surplus food. Part IV. A comparative analysis of Parus atricapillus L., P.cristatus L. and P. ater L. , 2012 .

[2]  D. Ph.,et al.  Black-capped Chickadee , 2011 .

[3]  F. Miller,et al.  Home at last: neural stem cell niches defined. , 2009, Cell stem cell.

[4]  Howard Eichenbaum,et al.  The neurobiology of memory based predictions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  L. LaDage,et al.  Effects of captivity and memory-based experiences on the hippocampus in mountain chickadees. , 2009, Behavioral neuroscience.

[6]  D. Sherry,et al.  The seasonal hippocampus of food-storing birds , 2009, Behavioural Processes.

[7]  T. Roth,et al.  Hippocampal volumes and neuron numbers increase along a gradient of environmental harshness: a large-scale comparison , 2009, Proceedings of the Royal Society B: Biological Sciences.

[8]  B. McEwen,et al.  Uncovering the mechanisms of estrogen effects on hippocampal function , 2008, Frontiers in Neuroendocrinology.

[9]  John R. Krebs,et al.  Retrieval of stored seeds by Marsh Tits Parus palustris in the field , 2008 .

[10]  Lucinda H. Male,et al.  Memory for food caches: not just for retrieval , 2007 .

[11]  D. Sherry,et al.  Greater hippocampal neuronal recruitment in food‐storing than in non‐food‐storing birds , 2007, Developmental neurobiology.

[12]  D. Sherry,et al.  Neurobiology of spatial behavior , 2007 .

[13]  Ken A. Otter,et al.  The ecology and behavior of chickadees and titmice : an integrated approach , 2007 .

[14]  V. Tropepe,et al.  A comparative framework for understanding the biological principles of adult neurogenesis , 2006, Progress in Neurobiology.

[15]  D. Sherry,et al.  Annual Cycle of the Black-Capped Chickadee: Seasonality of Food-Storing and the Hippocampus , 2006, Brain, Behavior and Evolution.

[16]  V. Pravosudov,et al.  The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison , 2006, Proceedings of the Royal Society B: Biological Sciences.

[17]  V. Pravosudov On seasonality in food-storing behaviour in parids: do we know the whole story? , 2006, Animal Behaviour.

[18]  Τ.V. Smulders, A Multi-disciplinary Approach to Understanding Hippocampal Function in Foodhoarding Birds , 2006, Reviews in the neurosciences.

[19]  J. Erichsen,et al.  Representing the Richness of Avian Spatial Cognition: Properties of a Lateralized Homing Pigeon Hippocampus , 2006, Reviews in the neurosciences.

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

[21]  An examination of avian hippocampal neurogenesis in relationship to photoperiod , 2005, Neuroreport.

[22]  E. A. MacDougall-Shackleton,et al.  Effects of day-length and food availability on food caching, mass and fat reserves in black-capped chickadees (Poecile atricapillus) , 2005, Physiology & Behavior.

[23]  A. Hansen,et al.  Influence of season and environment on adult neurogenesis in the central olfactory pathway of the shore crab, Carcinus maenas , 2004, Brain Research.

[24]  Gerald E. Hough,et al.  Revised nomenclature for avian telencephalon and some related brainstem nuclei , 2004, The Journal of comparative neurology.

[25]  D. Sherry,et al.  Neuron production, neuron number, and structure size are seasonally stable in the hippocampus of the food-storing black-capped chickadee (Poecile atricapillus). , 2004, Behavioral neuroscience.

[26]  Jürgen Winkler,et al.  Transient expression of doublecortin during adult neurogenesis , 2003, The Journal of comparative neurology.

[27]  F. Doetsch,et al.  The glial identity of neural stem cells , 2003, Nature Neuroscience.

[28]  S. Shettleworth Memory and Hippocampal Specialization in Food-Storing Birds: Challenges for Research on Comparative Cognition , 2003, Brain, Behavior and Evolution.

[29]  D. Sherry,et al.  Photoperiodic regulation of food storing and hippocampus volume in black-capped chickadees, Poecile atricapillus , 2003, Animal Behaviour.

[30]  J. García-Verdugo,et al.  The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals , 2002, Brain Research Bulletin.

[31]  F. Rodríguez,et al.  Spatial memory and hippocampal pallium through vertebrate evolution: insights from reptiles and teleost fish , 2002, Brain Research Bulletin.

[32]  G. S. Morato,et al.  Effects of intracerebroventricular administration of 7-nitroindazole on tolerance to ethanol , 2002, Brain Research Bulletin.

[33]  Gregory F Ball,et al.  Photoperiodic Control of Seasonality in Birds , 2001, Journal of biological rhythms.

[34]  R. McKay,et al.  Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus , 2001, The Journal of comparative neurology.

[35]  T. Smulders,et al.  Effects of captivity and testosterone on the volumes of four brain regions in the dark-eyed junco (Junco hyemalis). , 2000, Journal of neurobiology.

[36]  Eliot A. Brenowitz,et al.  Seasonal plasticity in the adult brain , 2000, Trends in Neurosciences.

[37]  Johannes Gerdes,et al.  The Ki‐67 protein: From the known and the unknown , 2000, Journal of cellular physiology.

[38]  F. Nottebohm,et al.  Fate of new neurons in adult canary high vocal center during the first 30 days after their formation , 1999, The Journal of comparative neurology.

[39]  E. Gould,et al.  Learning enhances adult neurogenesis in the hippocampal formation , 1999, Nature Neuroscience.

[40]  Gerd Kempermann,et al.  Experience-Induced Neurogenesis in the Senescent Dentate Gyrus , 1998, The Journal of Neuroscience.

[41]  J. García-Verdugo,et al.  Primary Neural Precursors and Intermitotic Nuclear Migration in the Ventricular Zone of Adult Canaries , 1998, The Journal of Neuroscience.

[42]  J. Summers-Smith House Sparrow , 1997, Birds of Houston.

[43]  A. Dhondt,et al.  How much memory do tits need? , 1997, Trends in ecology & evolution.

[44]  V. Pravosudov,et al.  Management of fat reserves and food caches in tufted titmice (Parus bicolor) in relation to unpredictable food supply , 1997 .

[45]  C. Clark,et al.  Long-term hoarding in the Paridae: a dynamic model , 1997 .

[46]  S. Shettleworth,et al.  Hippocampal lesions impair memory for location but not color in passerine birds. , 1996, Behavioral neuroscience.

[47]  F. Nottebohm,et al.  Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Russell P. Balda,et al.  Predicting Cognitive Capacity from Natural History: Examples from Four Species of Corvids , 1996 .

[49]  J. Krebs,et al.  Effects of photoperiod on food‐storing and the hippocampus in birds , 1995, Neuroreport.

[50]  T. Smulders,et al.  Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. , 1995, Journal of neurobiology.

[51]  S. Shettleworth,et al.  Effects of season and photoperiod on food storing by black-capped chickadees, Parus atricapillus , 1995, Animal Behaviour.

[52]  J. Ekman,et al.  Benefits of food hoarding , 1994, Nature.

[53]  F. Nottebohm,et al.  Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[54]  J. Lucas Regulation of cache stores and body mass in Carolina chickadees (Panes carolinensis) , 1994 .

[55]  Lynda Peterson,et al.  The effects of time constraints and changes in body mass and satiation on the simultaneous expression of caching and diet-choice decisions , 1993, Animal Behaviour.

[56]  T. A. Hurly,et al.  Energetic reserves of marsh tits (Parus palustris): food and fat storage in response to variable food supply , 1992 .

[57]  R. Hope-Simpson The Influence of Season , 1992 .

[58]  Andy Purvis,et al.  Comparative methods for explaining adaptations , 1991, Nature.

[59]  J. Lucas,et al.  When should chickadees hoard food? Theory and experimental results , 1991, Animal Behaviour.

[60]  J. Krebs,et al.  Why hoard? The economics of food storing in tits, Parus spp. , 1990 .

[61]  Fernando Nottebohm,et al.  Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division , 1990, Neuron.

[62]  David F. Sherry,et al.  Hippocampus and memory for food caches in black-capped chickadees , 1989 .

[63]  S. Healy,et al.  Hippocampal specialization of food-storing birds. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[64]  D. Sherry,et al.  The hippocampal complex of food-storing birds. , 1989, Brain, behavior and evolution.

[65]  Fernando Nottebohm,et al.  Migration of young neurons in adult avian brain , 1988, Nature.

[66]  F. Nottebohm,et al.  Mapping of radial glia and of a new cell type in adult canary brain , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[67]  N. Kuroda A Distributional Analysis of Diomedea immutabilis and D. nigripes in the North Pacific , 1988 .

[68]  Food Storing Behaviour of Willow Tit Parus montanus , 1988 .

[69]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[70]  John R. Krebs,et al.  Food storing by marsh tits , 1981, Animal Behaviour.

[71]  Df. Tomback,et al.  Foraging strategies of Clark's nutcracker , 1978 .

[72]  E. Odum Annual Cycle of the Black-Capped Chickadee: 3 , 1942 .

[73]  A. Kappers Avian brains and a new understanding of vertebrate brain evolution , 2022 .