School of Psychology, Birkbeck College

Course PSYC044U (Psychobiology II.) WEEK 9
March 22, 2007

gifThis is just the first 9 pages of the longer paper handout. Web versions of the other pages in the paper handout (and additional items not on the handout) are accessible from the side index. If you need to print out the handout, then all the pages are in this 'pdf' file, but this is quite large and may be difficult to download over a telephone modem.


Processes of animal memory: experimental analyses and anatomical and ecological theories


The simplest theoretical issue is whether “working memory” processes can be distinguished from mechanisms of response-habit learning and Pavlovian conditioning.

It must be pointed out that the term “memory” is often applied to all effects of previous experience on animal behaviour including the most basic forms of Pavlovian and Thorndikean conditioning (e.g. Kandel & Pittenger, 1999; Kandel, 2001). Distinctions can be drawn however between, for instance, transient sensory buffers; automatic associations; motor skills and response habits; long-term acquired knowledge (as in cognitive maps of local environments) and working memory systems (e.g. Roberts 1998). It has often been emphasised that in many forms of human amnesia, various kinds of perceptual and motor skill learning remains possible (Squire, 1992; Woodruff-Pak, 1993; Gabrieli et al, 1995; McKenna & Gerhand, 2002; Hikosaka et al., 2002). This suggests that the conditioning process is anatomically separate from other kinds of human memory, and there is evidence to support this from the use of methods in which brain activity is mapped or scanned during the performance of various cognitive tasks (e.g. Esteves et al, 1994; Bao et al., 2002; Courtney et al, 1998). There is also a measure of agreement that in human subjects it is possible to distinguish implicit (nonconscious) from explicit learning (e.g. Berry, 1994; Seger, 1994; Persaud et al., 2006) and declarative (verbally accessible) from non-declarative memory (Green and Woodruff-Pak, 1997; Squire and Zola, 1996; Eichenbaum, 1997, 2000; Poldrack & Packard, 2003: see also Brewin, 2001 in week 7 and p. 20 of this handout).

There are several particular kinds of behavioural experiment which have been used to support the concept of  “working memory in animals as something separate from the minimal associations necessary for basic conditioning in animal learning. Some of these are kinds of experiment are discussed briefly below.

In a change in terminology the data from same general kinds of experiments have recently been discussed as providing evidence for animal models of “episodic memory” (Aggleton and Brown, 1999; Griffiths, Dickinson and Clayton, 1999, Suzuki and Clayton, 2000 Morris, 2001, Tulving, 2002; Eacott et al., 2005; Babb & Crystal, 2006 — “declarative memory system” is also used the same context: Eichenbaum, 1997, 2000).

The general conclusion is that there are distinctions to be drawn between memory for recent events and the associative learning of skills and habits, and that some (but not all) aspects of this distinction apply to both human and animal memory (Kesner & Hopkins, 2006; Eichenbaum, 1997, 2000; Manns & Eichenbaum, 2006; Courtney et al;1998; Suzuki and Clayton, 2000; Morris, 2001 Poldrack & Packard, 2003; Wishaw & Wallace, 2003; Pasternak & Greenlee, 2005).


Sample Essay

Discuss experimental evidence and the theoretical background for the distinction between memory for recent events and response learning in animal behaviour.










[bottom of page 1 of wk 9 handout]
Working memory and the radial maze

Olton and Samuelson (1976) introduced a technique which appears to test rats’ memories of where they have recently been. On each daily trial animals are placed at the centre of a series of spokes, referred to as “arms” of the maze. A small amount of food is available (out of sight) at the end of each arm. The most efficient strategy would be for a rat to travel down each arm of the maze just once, retrieving all the available food with the minimum distance travelled. This is indeed the strategy adopted: Olton and Samuelson (1976) found that, after 40 trials, rats chose on average 7.5 different arms of the possible 8 arms of the maze in their first 8 choices. Control experiments established that the animals were not using odour cues to accomplish this efficient strategy. (Rats continue to behave as though they are choosing different geographical places when they are confined to the centre of the maze after returning from each choice, under conditions which allow the experimenters to swop visited and un-visited arms between choices: Olton and Collison, 1979).

This and other evidence suggests that the animals use fairly distant landmarks (“extra-maze cues”) to distinguish between different parts of the maze, and either remember the places they have been in an overall “cognitive map” of the maze, or have memories organised like “lists” of individual already visited places (Brown, 1992).

[top of page 2 of handout]

The use of radial (and other) mazes allows a distinction to be made between “reference memory” and “working memory”. (e.g. Olton, 1979). Reference memory applies to relatively permanent features of the environment, such as the location of the single goal in a conventional maze, or the position of rewarded arms in a radial maze where only half of the arms are baited each day (the same ones each time: Olton and Pappas, 1979). “Working memory” applies to the mechanism that enables a rat not to revisit arms already visited on a particular day. This form of memory is often linked to the functioning of the hippocampal system in both humans and animals (Scoville and Milner, 1957; Kesner, 1990; Bunsey and Eichenbaum, 1996; Eichenbaum, 1997, 2000; Morris, 2001).

It has been reported that children under the age of 7 perform poorly when tested in a suitably scaled up radial maze, the conclusion being drawn that human brain systems required for spatial memory of this kind are not fully developed until approximately 7 years of age. (Overman et al, 1996).

Spatial memory not involving food rewards can be tested with submerged platform tests: rats placed in a large tank learn to swim to the location of an invisible platform from variable starting positions, and can learn to make few errors after the first trial when the platform is moved to a different position each day. (Morris et al, 1982; Gerlai et al., 2002; Morris, 2001.)

Delayed Response Methods

Hunter (1913) tested various species in experiments in which a correct choice between a number of doors was indicated by a brief light above it, animals not being allowed to make the choice until a few seconds time later, and concluded that both rats and dogs solved this problem by maintaining bodily orientation (“pointing”) to the correct direction. However, when animals are shown food in a particular location, they may successfully find it after delays long enough to preclude this peripheral mechanism (Menzel, 1973; see Walker, 1985).

[bottom of page 2 of handout]
The Delayed-Matching-to-Sample Technique (DMTS)

A widely used experimental method also precludes the use of response perseveration as a mechanism, since it requires some form of memory of the properties of recent stimuli. Usually there is a 3-part visual display. On a central screen a “sample” stimulus is presented (animals being typically required to make an unrewarded response to the sample to ensure it has been noticed). There is then a delay period, which may be variable, before two different “choice” stimuli are presented at the same time on the outside screens, only one being the same as the most recent sample, the subjects being rewarded only if they choose this one. (See the diagram in Lieberman, 2000; page 379.) Since the sample is varied from trial, as is also the location, left or right, of the subsequent correct choice, successful performance must be interpreted as due to some kind of transient memory for the sample. The simplest theories propose that “stimulus traces” of the sample, which gradually decay, are used to direct choices, and in many experiments performance declines rapidly with delays longer than a few seconds (Roberts and Grant, 1976; D’Amato and Cox, 1976).

Such theories need to be elaborated however in order to account for proactive and retroactive interference effects (e.g. Overman and Doty, 1980), and superior performance for "surprising" (rare) samples (Lieberman, 2000; p. 380). These results suggest that what is remembered is not a passive sensory trace of the sample but a more active process. (See Morimura and Matsuzawa, 2001; Hampton, 2001)

A further result which can be obtained with this technique is the Serial Position Effect well known from studies of human memory. This is possible because animals can be trained to observe “lists” of samples (e.g. 10 pictures of human artifacts) before a delay, a choice being then presented between one item which was on the most recent list, and one which wasn’t (Sands and Wright, 1980; Wright et al, 1984; Castro and Larsen, 1992; Wright, 2002).

Naturalistic experiments on finding stored food.

It is difficult to ascribe an ecological function to the serial position effect obtained in memory for lists of objects, although it may reflect the operation of generally useful memory mechanisms. On the other hand it is possible to observe performance indicative of memory mechanisms which may be highly specialized in species which under natural conditions hoard food in multiple locations.

Textbooks on animal behaviour tend to suggest that squirrels find hoarded food by using their sense of smell, but it is an important aspect of their foraging (Wauters et al., 1995) and there are one or two suggestions that their visual spatial sense is also imporant in foraging (Devenport et al, 2000; Jacobs and Shiflett, 1999) and mate finding (Schwagmeyer et al., 2000).

[middle of page 3 of handout]

By contrast there is a very extensive literature on the importance of visual memory for the retrieval of hoarded food in several bird species. Shettleworth and Krebs (1982) studied the behaviour of marsh tits in an large aviary in which old tree branches had a total of 97 holes drilled in them, covered with cloth flaps. Birds accustomed to the aviary but kept elsewhere were placed in it with a bowl of hemp seeds available, and allowed to store 12 of the seeds in hiding places they selected, which took 7 or 8 minutes. They were then removed from the aviary for 2 or 3 hours, and returned to it with no food available apart from the 12 seeds they had stored. The average performance of four birds each given a 12 minute recovery test of this kind was 8 out of the 12 seeds recovered, from inspections of 30 of the 97 holes. On average, 5 out of the first 10 holes inspected contained seeds. Clearly this performance is not perfect, but it is very substantially better than chance.

[bottom of page 10 of handout]

Observations of Clark’s Nutcracker (a North American corvid — crow-like bird) suggests that an individual bird may store up to 30,000 pine nuts in 2,500 locations during the autumn, returning to these locations throughout the winter, and in some cases much later in the following year. Experiments on captive birds of these species indicated that non-local landmarks are used in coding the location of food-stores, since they made systematic errors if obvious features of the test environment, such as logs or large stones, were moved during the retention interval (Balda and Turek, 1984; Kamil and Balda, 1985; Gouldbeierle and Kamil, 1996, 1999; Bednekoff and Balda, 1996). Laboratory experiments on scrub jays (summarised by Griffiths et al., 1999 see also Clayton et al., 2001; 2003 and Dally et al., 2006) suggest that they remember “when” and “what” as well as “where” in the context of food storing episodes.

The theoretical issue of the role of the hippocampus

Experiments using all the above behavioural tests, and neuroanatomical surveys, have been performed to investigate the role of the hippocampus in animal memory. As hippocampal damage has long been identified with deficits in some kinds of memory in humans (Scoville and Milner, 1957; Woodruff-Pak, 1993) the analogy between human and animal memory is strengthened if specific deficits on memory related tasks can be demonstrated.

Large numbers of experiments on a variety of tasks show behavioural deficits as a consequence of damage to the hippocampal system. The dispute between those who have examined this data is whether the deficits arise from interference with storage of geographical information (O’Keefe and Nadel, 1978; Lever et al,. 2002) or whether they arise from impairments of a domain-neutral working memory system (Olton, 1979; Eichenbaum, 1997, 2000)). The dispute is difficult to resolve, because so many of the tasks used, especially with rats, have a spatial component. However, the two possibilities are not mutually exclusive (Kesner, 1990). The fact that performance impairments are found with tasks which lack an obvious geographical component is compatible with the position that the hippocampal formation in most species codes both spatial and temporal aspects of recent events (Kesner, 1990; Busner and Eichenbaum, 1996; Eichenbaum, 1997, 2003; Furusawa et al., 2006). Although O’Keefe, 1999 continues to maintain the position that the hippocampus should be regarded solely as a cognitive map, at least in rats, most discussions of the human hippocampus assume that it has more varied functions: Hoffman & McNaughton, 2002; Manns et al., 2003; Eichenbaum, 1997, 2000, 2003; Fortin et al., 2002, 2004).

Anatomical and ecological issues in theories of animal memory are combined in studies which examine the role of the hippocampus in species with specialized memory functions. Sherry et al (1989), Krebs et al (1989) and Healy and Krebs (1993) concluded that the relative size of the hippocampal complex is larger in food-storing birds than in comparison species (supported by Maguire et al. 2000, Shors et al. 2001 Clayton, 2001,Susuki & Clayton, 2001, Lucas et al., 2004 and Healy et al., 2005 but contested by Bolhuis & Macphail, 2001 and Brodin and Lundborg, 2003) . Sherry and Vaccarino (1989) found that hippocampal lesions impaired birds' abilities to recover food from caches, without impairing recovery of food from sites labelled with distinctive cues. While the literature on homing in pigeons lacks a clear consensus, there have been suggestions (e.g. Gagliardi et al, 1999; 2002) that the hippocampus has an important role in some aspects of this complex geographic skill and in particular for the recognition of visual landmarks.


  • Several sources of evidence indicate that animals may make use of memory processes which involve temporary storage of recent information, which are not necessarily tied to any given response output and which therefore can be distinguished from response skills, impulses or habits. Memory for the presence or absence of food items at certain spatial locations is a significant example, but other procedures, such as Delayed Matching to Sample, show temporary memories for non-spatial features of recent stimuli.
  • Memory about food sources would have obvious functional value for the achievement of optimum foraging strategies in many species, and the ability of individuals in food-storing species to find food they have hidden themselves has been subjected to experimental tests.
  • Considerable attention has been paid to the importance of the hippocampal formation for performance of tasks intended to tap working memory, and although there is disagreement about its precise function, in particular the degree to which it is specialized for spatial information, there is some degree of consensus that this brain structure “plays an important role in mediating mnemonic functions” and that “there are significant parallels across species” in this (Kesner, 1990; p.200; see also Squire, 1992; Eichenbaum, 1997; Maguire et al, 2000; Grön et al, 2000; Morris, 2001; O'Reilly & Norman, 2002; Poldrack & Packard, 2003; O'Reilly & Norman, 2002; Poldrack & Packard, 2003; Ekstrom et al., 2003; Ferbinteanu & Shapiro, 2003; Hori et al., 2005; Manns & Eichenbaum, 2006; Suzuki, 2006).  


Main Sources

Walker, S.F. (1985). Animal Thought. Routledge & Kegan Paul: London. pp.287-326

Walker, S.F. (1987). Animal Learning: An Introduction. Routledge & Kegan Paul: London. pp. 302-332


Further Reading

Lieberman, D. (2000) Learning: Behavior and Cognition. Belmont: Wadsworth. (pp. 367-384)

Roberts, W.A (1998) Principles of Animal Cognition. Boston: McGraw-Hill. Chapter 3. “Working Memory: Early Research and Contemporary Procedures and Findings. (1 copy on short loan at BK; 4 loan copies)

Pearce J.M. (1997) Animal Learning and Cognition 2nd Edition. Hove: Psychology Press. Chapter 6 Part 2 “Memory: Short-term Retention”. (156.315 PEA in new section at Birkbeck. 1 normal and 1 Short Loan copy)


Other References (Not normally required for Further Reading).

Aggleton, J. P., & Brown, M. W. (1999). Episodic memory, amnesia and the hippocampal-anterior thalamic axis. Behavioral and Brain Sciences, 22(3), 425-489.

Albright, T. D., Kandel, E. R., & Posner, M. I. (2000). Cognitive neuroscience. Current Opinion in Neurobiology, 10(5), 612-624.

Alvarez, P, Zola-Morgan, S and Squire, L (1994) The animal-model of human amnesia - long-term-memory impaired and short-term-memory intact. Proceedings of the National Academy of Sciences of the United States of America, Vol.91, No.12, Pp.5637-5641

www.pdf version of this paper(log on first for for access outside the College)

Babb, S. J., & Crystal, J. D. (2005). Discrimination of what, when, and where: Implications for episodic-like memory in rats. Learning and Motivation, 36(2), 177-189.

Babb, S. J., & Crystal, J. D. (2006). Episodic-like memory in the rat. Current Biology, 16(13), 1317-1321.

Balda, R.P. and Turek, R.J. (1984) The cache-recovery system as an example of memory capabilities in Clark's nutcracker. In Roitblat, H. L., Bever, T.G. and Terrace, H.S. (eds.) Animal Cognition. LEA: London, 513-32.

Bao, S. W., Chen, L., Kim, J. J., & Thompson, R. F. (2002). Cerebellar cortical inhibition and classical eyeblink conditioning. Proc. of the National Academy of Sciences of the United States of America, 99(3), 1592-1597.

Barkley, C. L., & Jacobs, L. F. (2007). Sex and species differences in spatial memory in food-storing kangaroo rats. Animal Behaviour, 73, 321-329.

Bednekoff, PA and Balda, RP (1996) Observational spatial memory in Clarks Nutcrackers and Mexican Jays. Animal Behaviour, Vol.52, No.Pt4, Pp.833-839 .

Benhamou, S., Bried, J., Bonadonna, F., & Jouventin, P. (2003). Homing in pelagic birds: a pilot experiment with white-chinned petrels released in the open sea. Behavioural Processes, 61(1-2), 95-100.

Bennett, M. R., & Hacker, P. M. S. (2001). Perception and memory in neuroscience: a conceptual analysis. Progress in Neurobiology, 65(6), 499-543.

Berry, DC (1994) Implicit learning - 25 years on - a tutorial. Attention and Performance, Vol.15, Pp.755-782.

Biegler, R., McGregor, A., Krebs, J. R., & Healy, S. D. (2001). A larger hippocampus is associated with longer-lasting spatial memory. Proc. of the National Academy of Sciences of the United States of America, 98(12), 6941-6944.

Bingman, V.P. and Yates, G. (1992) Hippocampal lesions impair navigational learning in experienced homing pigeons. Behavioural Neuroscience, 106, 229-232.

Blaizot, X., Landeau, B., Baron, J. C., & Chavoix, C. (2000). Mapping the visual recognition memory network with PET in the behaving baboon. Journal of Cerebral Blood Flow and Metabolism, 20(2), 213-219.

Bolhuis, J. J., & Macphail, E. M. (2001). A critique of the neuroecology of learning and memory. Trends in Cognitive Sciences, 4(10), 426-433.

Brodin, A., & Lundborg, K. (2003). Is hippocampal volume affected by specialization for food hoarding in birds? Proceedings of the Royal Society of London Series B-Biological Sciences, 270(1524), 1555-1563.

Brown, M.F. (1992) Does a cognitive map guide choices in the radial arm maze? Journal of Experimental Psychology: Animal Behaviour Processes, 18, 56-66.

Bucan, M., & Abel, T. (2002). The mouse: Genetics meets behaviour. Nature Reviews Genetics, 3(2), 114-123.

Buchanan, J.P., Gill, T.V., and Braggio, J.T. (1981) Serial position and clustering effects in chimpanze's 'free recall'. Memory and Cognition, 9, 651-60.

Buckmaster, C. A., Eichenbaum, H., Amaral, D. G., Suzuki, W. A., & Rapp, P. R. (2004). Entorhinal cortex lesions disrupt the relational organization of memory in monkeys. Journal of Neuroscience, 24(44), 9811-9825.

Buffalo, B, Gaffan, D, Murray, EA ( 1994) A primacy effect in monkeys when list position is relevant. Quarterly Journal of Experimental Psychology Section B-Comparative And Physiological Psychology, , Vol.47, No.4, Pp.353-369

Bunsey, M and Eichenbaum, H (1996) Conservation of hippocampal memory function in rats and humans. Nature, Vol.379, No.6562, Pp.255-257.

Burgess, N. (2002). The hippocampus, space, and viewpoints in episodic memory. Quarterly Journal of Experimental Psychology Section a-Human Experimental Psychology, 55(4), 1057-1080.

Cain, D. P., Finlayson, C., Boon, F., & Beiko, J. (2002). Ethanol impairs behavioral strategy use in naive rats but does not prevent spatial learning in the water maze in pretrained rats. Psychopharmacology, 164(1), 1-9.

Carter, R. M., Hofstotter, C., Tsuchiya, N., & Koch, C. (2003). Working memory and fear conditioning. Proceedings of the National Academy of Sciences of the United States of America, 100(3), 1399-1404.

Cassaday, HJ, and Rawlins, JNP (1997) The hippocampus, objects, and their contexts. Behavioral Neuroscience, Vol.111, No.6, Pp.1228-1244.

Castro, C.A. and Larsen, T. (1992) Primacy and recency effects in nonhuman primates. Journal of Experimental Psychology: Animal Behaviour Processes, 18, 335-340.

Clayton, N. S. (2001). Hippocampal growth and maintenance depend on food-caching experience in juvenile mountain chickadees (Poecile gambeli). Behavioral Neuroscience, 115(3), 614-625.

Clayton, N. S., & Dickinson, A. (1999). Scrub jays (Aphelocoma coerulescens) remember the relative time of caching as well as the location and content of their caches. Journal of Comparative Psychology, 113(4), 403-416.

Clayton, N. S., Griffiths, D. P., Emery, N. J., & Dickinson, A. (2001). Elements of episodic-like memory in animals. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 356(1413), 1483-1491.

Clayton, N. S., Yu, K. S., & Dickinson, A. (2001). Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes. Journal of Experimental Psychology-Anim, Beh. Processes, 27(1), 17-29.

Clayton, N. S., Yu, K. S., & Dickinson, A. (2003). Interacting cache memories: Evidence for flexible memory use by Western Scrub-Jays (Aphelocoma californica). Journal of Exp. Psychology-Anim Beh Proc, 29(1), 14-22.

Clayton, NS and Dickinson, A (1998) Episodic-like memory during cache recovery by scrub jays. Nature, Vol.395, No.6699, Pp.272-274.

Clayton, NS, Dickinson, A (1999) Memory for the content of caches by scrub jays (Aphelocoma coerulescens). Journal of Experimental Psychology-Animal Behavior Processes, Vol.25, No.1, Pp.82-91.

Clayton, NS, Krebs, JR (1994) One-trial associative memory - comparison of food-storing and nonstoring species of birds. Animal Learning and Behavior, Vol.22, No.4, Pp.366-372

Cohen, T. E., Kaplan, S. W., Kandel, E. R., & Hawkins, R. D. (1997). A simplified preparation for relating cellular events to behavior: Mechanisms contributing to habituation, dishabituation, and sensitization of the Aplysia gill- withdrawal reflex. Journal of Neuroscience, 17(8), 2886-2899.

Colombo, M., & Broadbent, N. (2000). Is the avian hippocampus a functional homologue of the mammalian hippocampus? Neuroscience and Biobehavioral Reviews, 24(4), 465-484.

Courtney, SM, Petit, L, Maisog, JM, Ungerleider, LG, and Haxby, JV (1998) An area specialized for spatial working memory in human frontal cortex. Science, Vol.279, No.5355, Pp.1347-1351.

Crowley, P. H. (2001). Dangerous games and the emergence of social structure: evolving memory-based strategies for the generalized hawk-dove game. Behavioral Ecology, 12(6), 753-760.

D'Amato, M.R. and Cox, J.K. (1976) Delay of consequences and short-term memory in monkeys. In Medin, D.L., Roberts, D.A. and Davis, R.T. (eds.) Processes in Animal Memory. Lawrence Erlbaum Associates: Hillsdale, N.J., 49-78.

Dally, J. M., Clayton, N. S., & Emery, N. J. (2006). The behaviour and evolution of cache protection and pilferage. Animal Behaviour, 72, 13-23.

Dally, J. M., Emery, N. J., & Clayton, N. S. (2004). Cache protection strategies by western scrub-jays (Aphelocoma californica): hiding food in the shade. Proc. of the Royal Soc of London B-Biological Sciences, 271, S387-S390.

Dally, J. M., Emery, N. J., & Clayton, N. S. (2006). Food-caching western scrub-jays keep track of who was watching when. Science, 312(5780), 1662-1665.

Day, LB, Crews, D and Wilczynski, W (1999) Spatial and reversal learning in congeneric lizards with different foraging strategies. Animal Behaviour, Vol.57, No.Pt2, Pp.393-407.

de Hoz, L., & Wood, E. R. (2006). Dissociating the past from the present in the activity of place cells. Hippocampus, 16(9), 704-715.

Devenport, J. A., Luna, L. D., & Devenport, L. D. (2000). Placement, retrieval, and memory of caches by thirteen-lined ground squirrels. Ethology, 106(2), 171-183.

D'Hooge, R., & De Deyn, P. P. (2001). Applications of the Morris water maze in the study of learning and memory. Brain Research Reviews, 36(1), 60-90.

Dobbins, I. G., Rice, H. J., Wagner, A. D., & Schacter, D. L. (2003). Memory orientation and success: separable neurocognitive components underlying episodic recognition. Neuropsychologia, 41(3), 318-333.

Dragoi, G., & Buzsaki, G. (2006). Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies. Neuron, 50(1), 145-157.

Eacott, M. J., Easton, A., & Zinkivskay, A. (2005). Recollection in an episodic-like memory task in the rat. Learning & Memory, 12(3), 221-223.

Easton, A., & Gaffan, D. (2000). Comparison of perirhinal cortex ablation and crossed unilateral lesions of the medial forebrain bundle from the inferior temporal cortex in the rhesus monkey: Effects on learning and retrieval. Behavioral Neuroscience, 114(6), 1041-1057.

Eichenbaum, H (1997) Declarative memory: insights from cognitive neurobiology. Annual Review of Psychology, Vol.48, Pp.547-572.

Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience, 1(1), 41-50.

Eichenbaum, H. (2000). Hippocampus: Mapping or memory? Current Biology, 10(21), R785-R787.

www.pdf version of this paper(log on first for for access outside the College)

Eichenbaum, H. (2003). How does the hippocampus contribute to memory? Trends in Cognitive Sciences, 7(10), 427-429.

Eichenbaum, H. (2004). Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron, 44(1), 109-120.

Ekstrom, A. D., Kahana, M. J., Caplan, J. B., Fields, T. A., Isham, E. A., Newman, E. L., & Fried, I. (2003). Cellular networks underlying human spatial navigation. Nature, 425(6954), 184-187.

Emery, N. J., & Clayton, N. S. (2001). Effects of experience and social context on prospective caching strategies by scrub jays. Nature, 414(6862), 443-446.

Emery, N. J., Dally, J. M., & Clayton, N. S. (2004). Western scrub-jays (Aphelocoma californica) use cognitive strategies to protect their caches from thieving conspecifics. Animal Cognition, 7(1), 37-43.

Esteves F, Parra C, Dimberg U, and Ohman, A (1994) Nonconscious associative learning: Pavlovian conditioning of skin conductance responses to masked fear-relevant facial stimuli. Psychophysiology, 31 No.4 pp.375-385

Faber, K. M., & Johnson, L. N. (2003). Hallucinating the past: A case of spontaneous and involuntary recall of long-term memories - Perspectives on the hemispheric organization of visual memory. Journal of Neurology, 250(1), 55-62.

Fabiani, M., Stadler, M. A., & Wessels, P. M. (2000). True but not false memories produce a sensory signature in human lateralized brain potentials. Journal of Cognitive Neuroscience, 12(6), 941-949.

Ferbinteanu, J., & Shapiro, M. L. (2003). Prospective and retrospective memory coding in the hippocampus. Neuron, 40(6), 1227-1239.

Fortin, N. J., Agster, K. L., & Eichenbaum, H. B. (2002). Critical role of the hippocampus in memory for sequences of events. Nature Neuroscience, 5(5), 458-462.

Fortin, N. J., Wright, S. P., & Eichenbaum, H. (2004). Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature, 431(7005), 188-191.

Fosse, M. J., Fosse, R., Hobson, J. A., & Stickgold, R. J. (2003). Dreaming and episodic memory: A functional dissociation? Journal of Cognitive Neuroscience, 15(1), 1-9.

Foster, D. J., & Wilson, M. A. (2006). Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature, 440(7084), 680-683.

Frick, RW and Lee, YS (1995) Implicit learning and concept-learning. Quarterly Journal of Experimental Psychology Section A-Human Experimental Psychology, Vol.48, No.3, Pp.762-782.

Furusawa, A. A., Hori, E., Umeno, K., Tabuchi, E., Ono, T., & Nishijo, H. (2006). Unambiguous representation of overlapping serial events in the rat hippocampal formation. Neuroscience, 137(2), 685-698.

Gabrieli, JDE, Carrillo, MC, Cermak, LS, McGlincheyberroth, R, Gluck, MA and Disterhoft, JF (1995) Intact delay-eyeblink classical-conditioning in amnesia. Behavioral Neuroscience, Vol.109, No.5, Pp.819-827

Gaffan, D (1994) Scene-specific memory for objects - a model of episodic memory impairment in monkeys with fornix transection, Journal of Cognitive Neuroscience, Vol.6, No.4, Pp.305-320

Gaffan, D (1996) Memory, action and the corpus striatum - current developments in the memory-habit distinction. Seminars in the Neurosciences, Vol.8, No.1, Pp.33-38.

Gagliardo, A., Ioale, P., Odetti, F., & Bingman, V. P. (2001). The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period. Proceedings of the Royal Society of London Series B-Biological Sciences, 268(1463), 197-202.

Gagliardo, A., Odetti, F., Ioale, P., Bingman, V. P., Tuttle, S., & Vallortigara, G. (2002). Bilateral participation of the hippocampus in familiar landmark navigation by homing pigeons. Behavioural Brain Research, 136(1), 201-209.

Gerlai, R. T., McNamara, A., Williams, S., & Phillips, H. S. (2002). Hippocampal dysfunction and behavioral deficit in the water maze in mice: An unresolved issue? Brain Research Bulletin, 57(1), 3-9.

Glassman, R. B., Garvey, K. J., Elkins, K. M., Kasal, K. L., & et al. (1994). Spatial working memory score of humans in a large radial maze, similar to published score of rats, implies capacity close to the magical number 7 + 2. Brain Research Bulletin, 34(2), 151-159.

Glassman, R. B., Leniek, K. M., & Haegerich, T. M. (1998). Human working memory capacity is 7 + 2 in a radial maze with distracting interruption: Possible implication for neural mechanisms of declarative and implicit long-term memory. Brain Research Bulletin, 47(3), 249-256.

Gluck, MA and Myers, CE (1997) Psychobiological models of hippocampal function in learning and memory. Annual Review of Psychology, Vol.48, Pp.481-514.

Goldman-Rakic, PS (1996) Regional and cellular fractionation of working-memory. Proceedings of the National Academy of Sciences of the United States of America, Vol.93, No.24, Pp.13473-13480.

Gould, E., Reeves, A. J., Fallah, M., Tanapat, P., Gross, C. G., & Fuchs, E. (1999). Hippocampal neurogenesis in adult Old World primates. Proceedings of the National Academy of Sciences of the United States of America, 96(9), 5263-5267.

Gould, E., Reeves, A. J., Graziano, M. S. A., & Gross, C. G. (1999). Neurogenesis in the neocortex of adult primates. Science, 286(5439), 548-552.

Gould-Beierle, K. (2000). A comparison of four corvid species in a working and reference memory task using a radial maze. Journal of Comparative Psychology, 114(4), 347-356.

Gouldbeierle, KL and Kamil, AC (1996) The use of local and global cues by clark nutcrackers, nucifraga-columbiana. Animal Behaviour, Vol.52, No.Pt3, Pp.519-528.

Green, JT and Woodruff-Pak, DS (1997) Concurrent eyeblink classical conditioning and rotary pursuit performance: implications for independent nondeclarative memory systems. Neuropsychology, Vol.11, No.4, Pp.474-487.

Griffiths, D., Dickinson, A., & Clayton, N. (1999). Episodic memory: what can animals remember about their past? Trends in Cognitive Sciences, 3(2), 74-80.

Gross, C. G. (2000). Neurogenesis in the adult brain: death of a dogma. Nature Reviews Neuroscience, 1(1), 67-73.

Hampton, R. R. (2001). Rhesus monkeys know when they remember. Proceedings of the National Academy of Sciences of the United States of America, 98(9), 5359-5362.

www. version of this paper(log on first for for access outside the College)

Hampton, R. R., & Hampstead, B. M. (2006). Spontaneous behavior of a rhesus monkey (Macaca mulatta) during memory tests suggests memory awareness. Behavioural Processes, 72(2), 184-189.

Hampton, R. R., Hampstead, B. M., & Murray, E. A. (2005). Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where, but not when, in an open-field test of memory. Learning and Motivation, 36(2), 245-259.

Hampton, R. R., Zivin, A., & Murray, E. A. (2004). Rhesus monkeys (Macaca mulatta) discriminate between knowing and not knowing and collect information as needed before acting. Animal Cognition, 7(4), 239-246

Healy, S. D., de Kort, S. R., & Clayton, N. S. (2005). The hippocampus, spatial memory and food hoarding: a puzzle revisited. Trends in Ecology & Evolution, 20(1), 17-22.

Healy, S.D. and Krebs, J.R. (1993) Development of hippocampal specialisation in a food-storing bird. Behavioural Brain Research, 53, 127-131.

Healy, SD, Clayton, NS and Krebs, JR (1994) Development of hippocampal specialization in 2 species of tit (Parus spp). Behavioural Brain Research, Vol.61, No.1, Pp.23-28

Hikosaka, O., Rand, M. K., Nakamura, K., Miyachi, S., Kitaguchi, K., Sakai, K., Lu, X., & Shimo, Y. (2002). Long-term retention of motor skill in macaque monkeys and humans. Experimental Brain Research, 147(4), 494-504.

Hori, E., Nishio, Y., Kazui, K., Umeno, K., Tabuchi, E., Sasaki, K., et al. (2005). Place-related neural responses in the monkey hippocampal formation in a virtual space. Hippocampus, 15(8), 991-996.

Jacobs, L. F., & Shiflett, M. W. (1999). Spatial orientation on a vertical maze in free-ranging fox squirrels (Sciurus niger). Journal of Comparative Psychology, 113(2), 116-127.

Kamil, A.C. and Balda, R.P. (1985). Cache recovery and spatial memory in Clark's nutcrackers (Nucifraga columbiana). Journal of Experimental Psychology: Animal Behaviour Processes, 11, 95-111

Kandel, E. R. (2001). Neuroscience - The molecular biology of memory storage: A dialogue between genes and synapses. Science, 294(5544), 1030-1038.

Kandel, E. R., & Pittenger, C. (1999). The past, the future and the biology of memory storage. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 354(1392), 2027-2052.

Kesner, R. P., & Hopkins, R. O. (2006). Mnemonic functions of the hippocampus: A comparison between animals and humans. Biological Psychology, 73(1), 3-18.

Kesner, R.P. (1990) Learning and memory in rats with an emphasis on the role of the hippocampal formation. In Kesner, R.P. and Olton, D.S. (eds) Neurobiology of Comparative Cognition. Hove and London: LEA. 179-204.

Krebs, J.R., Sherry, D.F., Healy, S.D., Perry, V.H. and Vaccarino, A.L. (1989) Hippocampal specialization of food-storing birds. Proceedings of the National Academy of Sciences (USA), 86, 1388-1392.

Leaver, L. A., Hopewell, L., Caldwell, C., & Mallarky, L. (2007). Audience effects on food caching in grey squirrels (Sciurus carolinensis): evidence for pilferage avoidance strategies. Animal Cognition, 10(1), 23-27.

Lever, C., Wills, T., Cacucci, F., Burgess, N., & O'Keefe, J. (2002). Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature, 416(6876), 90-94.

Louie, K., & Wilson, M. A. (2001). Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron, 29 (1), 145-56.

Lucas, J. R., Brodin, A., de Kort, S. R., & Clayton, N. S. (2004). Does hippocampal size correlate with the degree of caching specialization? Proceedings of the Royal Society of London Series B-Biological Sciences, 271(1556), 2423-2429.

Maguire, E. A., Gadian, D. G., Johnsrude, I. S., Good, C. D., Ashburner, J., Frackowiak, R. S., & Frith, C. D. (2000). Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the National Academy of Sciences of the United States of America, 14, 14.

Manns, J. R., & Eichenbaum, H. (2006). Evolution of declarative memory. Hippocampus, 16(9), 795-808.

Manns, J. R., Hopkins, R. O., Reed, J. M., Kitchener, E. G., & Squire, L. R. (2003). Recognition memory and the human hippocampus. Neuron, 37(1), 171-180.

McKenna, P., & Gerhand, S. (2002). Preserved semantic learning in an amnesic patient. Cortex, 38(1), 37-58.

Menzel, E.W. (1973) Chimpanzee spatial memory organization. Science, 182, 943-5.

Menzel, E.W. (1978) Cognitive mapping in chimpanzees. In Hulse, S.H., Fowler, H. and Honig, W.K. (eds.), Cognitive Processes in Animal Behaviour. Lawrence Erlbaum Associates: Hillsdale, N.J., 375-422.

Morimura, N., & Matsuzawa, T. (2001). Memory of movies by chimpanzees (Pan troglodytes). Journal of Comparative Psychology, 115(2), 152-158.

Morris, R. G. M. (2001). Episodic-like memory in animals: psychological criteria, neural mechanisms and the value of episodic-like tasks to investigate animal models of neurodegenerative disease. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 356(1413), 1453-1465.

Morris, R.G.M., Garrud, P., Rawlins, J.N.P. and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-3.

Nader, K. (2003). Memory traces unbound. Trends in Neurosciences, 26(2), 65-72.

Nottebohm, F. (2002). Neuronal replacement in adult brain. Brain Research Bulletin, 57(6), 737-749.

O'Keefe, J. (1999). Do hippocampal pyramidal cells signal non-spatial as well as spatial information? Hippocampus, 9(4), 352-364.

O'Keefe, J. and Nadel, L. (1978). The Hippocampus as a Cognitive Map. Clarendon Press: Oxford.

Olton, D.S. (1979) Mazes, maps, and memory. American Psychologist, 34, 583-96.

Olton, D.S. and Papas, B.C. (1979). Spatial memory and hippocampal function. Neuropsychologia, 17, 669-82.

Olton, D.S. and Samuelson, R.J. (1976). Remembrance of places passed: spatial memory in rats. Journal of Experimental Psychology: Animal Behaviour Processes, 2, 97-116.

O'Reilly, R. C., & Norman, K. A. (2002). Hippocampal and neocortical contributions to memory: advances in the complementary learning systems framework. Trends in Cognitive Sciences, 6(12), 505-510.

Overman, W.H. and Doty, R.W. (1980) Prolonged visual memory in macaques and man. Neuroscience, 5, 1825-31.

Overman, WH, Pate, BJ, Moore, K and Peuster, A (1996) Ontogeny of place learning in children as measured in the radial arm maze, morris search task, and open field task. Behavioral Neuroscience, Vol.110, No.6, Pp.1205-1228.

Pasternak, T., & Greenlee, M. W. (2005). Working memory in primate sensory systems. Nature Reviews Neuroscience, 6(2), 97-107.

Persaud, N., McLeod, P., & Cowey, A. (2007). Post-decision wagering objectively measures awareness. 10(2), 257-261.

Poldrack, R. A., & Packard, M. G. (2003). Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia, 41(3), 245-251.

Prusky, G. T., Douglas, R. M., Nelson, L., Shabanpoor, A., & Sutherland, R. J. (2004). Visual memory task for rats reveals an essential role for hippocampus and perirhinal cortex. Proceedings of the National Academy of Sciences of the United States of America, 101(14), 5064-5068.

Reed, J. M., & Means, L. W. (2004). Human implicit memory for irrelevant dimension values is similar to rats' incidental memory in simultaneous discrimination tasks. Behavioural Processes, 67(3), 383-393.

Sands, S.F. and Wright, A.A. (1980). Serial probe recognition performance by a rhesus monkey and a human with 10- and 20-item lists. Journal of Experimental Psychology: Animal Behaviour Processes, 6, 386-96.

Schwagmeyer, P. L., Parker, G. A., & Mock, D. W. (1998). Information asymmetries among males: implications for fertilization success in the thirteen-lined ground squirrel. Proceedings of the Royal Society of London Series B-Biological Sciences, 265(1408), 1861-1865.

Scoville, W.B. and Milner, B. (1957) Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 20, 11-21.

Seger, CA (1994) Implicit learning. Psychological Bulletin, Vol.115, No.2, Pp.163-196.

Shapiro, M. L., & Ferbinteanu, J. (2006). Relative spike timing in pairs of hippocampal neurons distinguishes the beginning and end of journeys. PNAS, 103(11), 4287-4292.

Sherry, D.F. and Vaccarino, A.L. (1989) Hippocampus and memory for food caches in Black-Capped Chickadees. Behavioural Neuroscience, 103, 308-318.

Sherry, D.F., Vaccarino, A.L., Buckenham, K. and Herz, R.S. (1989) The hippocampal complex of food-storing birds. Brain, Behaviour and Evolution, 34, 308-317.

Shettleworth, S.J. and Krebs, J.R. (1982). How marsh tits find their hoards: the roles of site preference and spatial memory. Journal of Experimental Psychology: Animal Behaviour Processes, 8, 354-75.

Shettleworth, S.J. and Krebs, J.R. (1986). Stored and encountered seeds: a comparison of two spatial memory tasks in marsh tits and chickadees. Journal of Experimental Psychology: Animal Behaviour Processes, 12, 248-57.

Shors, T.J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., & Gould, E. (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature, vol 410, 372-376.

Slotnick, B. (2001). Animal cognition and the rat olfactory system. Trends in Cognitive Sciences, 5(5), 216-222.

Squire, L.R. (1992) Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99, 195-231.

Squire, LR and Zola, SM (1996) Structure and function of declarative and nondeclarative memory-systems. Proceedings of the National Academy of Sciences of the United States of America, Vol.93, No.24, Pp.13515-13522.

www.htm version of this paper (log on first for for access outside the College)

Suzuki, W. A. (2006). Encoding new episodes and making them stick. Neuron, 50(1), 19-21.

www.htm version of this paper (log on first for for access outside the College)

Suzuki, W. A., & Clayton, N. S. (2000). The hippocampus and memory: a comparative and ethological perspective. Current Opinion in Neurobiology, 10(6), 768-773.

www.htm version of this paper (log on first for for access outside the College)

Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53, 1-25.

Walker, J.A., and Olton, D.S. (1984) Fimbria-fornix lesions impair spatial working memory but not cognitive mapping. Behavioural Neuroscience, 98, 226-42.

Wauters, LA, Suhonen, J and Dhondt, AA (1995) Fitness consequences of hoarding behavior in the Eurasian red squirrel. Proceedings of the Royal Society of London Series B-Biological Sciences, Vol.262, No.1365, Pp.277-281

Whishaw, I. Q., & Wallace, D. G. (2003). On the origins of autobiographical memory. Behavioural Brain Research, 138(2), 113-119.

Wich, S. A., & de Vries, H. (2006). Male monkeys remember which group members have given alarm calls. Proceedings of the Royal Society B-Biological Sciences, 273(1587), 735-740.

Wilson, F. A. W., & Rolls, E. T. (2005). The primate amygdala and reinforcement: A dissociation between rule-based and associatively-mediated memory revealed in neuronal activity. Neuroscience, 133(4), 1061-1072.

Woodruff-Pak, D.S. (1993) Eyeblink classical conditioning in H.M.: Delay and trace paradigms, Behavioural Neuroscience, 107, 911-925.

Wright, A. A. (2002). Monkey auditory list memory: Tests with mixed and blocked retention delays. Animal Learning & Behavior, 30(2), 158-164.

Wright, A.A., Santiago, H.C., Sands, S.F. and Urcuioli, P.J. (1984b). Pigeon and monkey serial probe recognition: acquisition strategies, and serial position effects. In Roitblat, H. L., Bever, T.G. and Terrace, H.S. (eds.). Animal Cognition. Lawrence Erlbaum Associates: London, 353-73.