School of Psychology, Birkbeck College|
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
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).
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
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,
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).
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.
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
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.
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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)
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