of Spatial and Episodic Memory


Research Projects

    In this research group, we study the issues of spatial and episodic memory using various levels of analysis: from the evolutionary through the functional to the mechanistic.  To combine all these levels of analysis and investigate their interactions, we study food-hoarding birds.  These animals scatter hoard their food, meaning that they hide many food items in a variety of different locations.  They are later able to retrieve these items with surprising accuracy, relying at least partly on a well-developed spatial memory system.  They not only remember where items are hidden, but also what type of food was hidden, and when it was hidden.  These birds have a larger hippocampus (the brain area believed to be involved in this memory) than do other birds.  We are currently running a number of separate, but related research projects. 

Anybody interested in post-graduate or post-doctoral work in any of these projects should feel free to contact me at


 1) Evolution and ecological function of memory

    This project looks at what the ecological function of hoarding and cache memory is in tits (family Paridae).  We believe that tits hoard food over 2 time scales: for short-term retrieval (hours to days) and for long-term retrieval (weeks to months).  We have investigated the role of memory in both of these time-frames and the function of hoarding itself in the natural history of this species. 

    In order for caches to survive throughout winter so that they are available to the animals when they need them, the animals will need to distribute their caches in such a way as to minimize cache theft.  Lucinda Male, who obtained her PhD in my lab, showed that the more dispersed distributions are, the higher the probability is that more items in that distribution survive (Male & Smulders, 2007a).  She also showed that coal tits actively avoid caching new items too close to existing ones, and that they seem to use spatial memory in this process (Male & Smulders, 2007b).  This suggests that memory is important for seasonal cache distribution, in order to optimize cache survival.  We currently do not believe that memory is used to retrieve caches after many months, because we do not have any evidence for memories lasting that long (Male & Smulders, 2007c), and mathematical modelling has suggested that long-term retrieval is possible without memory for specific cache sites (Smulders, 1998).  

    In the short-term, retrieval undoubtedly happens mostly through exact memories for hoarding sites.  However, the function of short-term retrieval has been less clear.  Rowan Cockcroft, another former PhD student, tested a novel hypothesis about the adaptive function of short-term caches.  Current dogma suggests that caches can act as an alternative to fat reserves, as they are readily available (using memory), yet do not have to be carried around on the body.  The alternative hypothesis we are testing is that caches are actually required to be able to produce fat reserves, because they allow the birds to eat at a constant rate, and keep the digestive tract working at highest efficiency.  We call this the "external crop" hypothesis.  Rowan's data clearly show that the stomach content of tits is limited, and that temporary access to abundant food resources does not allow the birds to eat as much food as needed to keep their energy reserves up.  If they are allowed to hoard, however, they can eat more food during the times that there is no access to the abundant food resource and therefore put on more energy reserves.  One still ongoing aspect of this project is the use of a stochastic dynamic model designed to ascertain the effect of a limited digestive tract size on the adaptive value of short-term hoarding.


coaltit02Andy Bright.jpg 2) Mechanisms underlying the motivation to hoard.

    What makes birds start to hoard, or hoard more or less, is still not completely resolved.  Shorter daylengths induce hoarding in a laboratory situation and unpredictable food supplies also increase hoarding intensity.  But what are the physiological mechanisms through which these environmental factors are transduced into behavioural changes? Because hoarding behaviour is tied to feeding, Rowan Cockcroft also investigated the role of appetite-regulating hormones on hoarding behaviour. He found that leptin injections suppress both eating and hoarding (manuscript in preparation).  Leptin is known in mammals to signal high fat reserves and suppress appetite.  Another appetite-regulating hormone, ghrelin, was also investigated, but its effects are currently ambiguous.  These results will form the basis of a more detailed examination of the interplay between appetite, hormones and hoarding behaviour.  In part to help with this investigation, we have obtained funding for 4 climate-controlled chambers in which we can control temperature and photoperiod independently in order to further investigate these questions.  Some of this work is done in collaboration with Dr. Tim Boswell.


 3) Neural mechanisms underlying large-scale memory processing.

    In 1995, in collaboration with Prof. Timothy DeVoogd, I found that the hippocampus of black-capped chickadees increased in size in the autumn (Smulders et al. 1995), which is the time of year when they do most of their food storing.  This increase in volume seemed at least in part due to an increase in the total number of neurons in the hippocampus (Smulders et al. 2000).  The goal of this research project is to investigate in more detail how this neuronal turnover is regulated.  We are doing this by closely following wild populations of willow tits (hoarders) and great tits (non-hoarders) in the field in Oulu (Finland), and collecting samples at different times of the year.  These brains will then be processed to count newly generated neurons and dying neurons.  With additional measures of hormone titers and of behaviour in the field, we hope to obtain a better idea of what it is that drives these seasonal changes.  By comparing food-hoarding birds to closely related non-hoarders, we'll also have a better idea whether the changes are really related to food-hoarding or a more general mechanism of dealing with oncoming winter scarcity.  The research is conducted in collaboration with Prof. Markku Orell of the University of Oulu in Finland.  The research was funded by the BBSRC.  Our preliminary results agree with our previously published work, and we are following up with projects in collaboration with Drs. Kazuo Okanoya and Jun Aruga of the RIKEN Brain Science Institute.


4) The role of the avian hippocampus in declarative-like memory

    Humans can recall when they experienced a certain episode, where this was and what exactly took place. This is generally referred to as episodic memory.  Because animals cannot tell us whether they remember all these details, it is difficult to investigate whether animals (a) have episodic memory and (b) which neural structures underlie this memory.  Food-hoarding birds have been shown to remember not only where they stored food, but what type of food was stored there and how long ago they stored it.  This finding was published in Nature in 1998 by Nicky Clayton and Tony Dickinson.  Former PhD student Ann Zinkivskay replicated and extended these findings in our laboratory using magpies (Zinkivskay et al, 2009).

   The ultimate goal of all this is to investigate the role of the avian hippocampal formation in this type of memory. We will approach this from two different angles.  One angle will be to investigate the importance of different sub-regions of the avian hippocampal formation by way of temporary local inactivation studies.  The second approach will be to record from multiple single neurons in the hippocampus of food-hoarding magpies while they are hoarding and retrieving different food-types.  We will then analyse the firing patterns of the neuronal ensembles to investigate whether not only spatial information is encoded in them, but also information about what was stored, and when it was stored.  We are actively pursuing funding for these projects at this time.  As part of this effort, I collaborate with Dr. V. Anne Smith on analysis techniques for multi-electrode array recordings (e.g. Smith et al 2006), a project that is part of the CARMEN project, funded by the EPSRC.


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Page last updated on 16 June 2009