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physiological mechanisms
BEHAVIORAL AND NEURAL BIOLOGY
33, 402-418 (1981)
Problem Solving in the Rat: Cognitive/Physiological Mechanisms 1 PAUL ELLEN AND STEVEN ANSCHEL
Department of Psychology, Georgia State University, Atlanta, Georgia 30303 Three bodies of data pertaining to the role of cognitive maps in animal problem solving are examined. First, it is shown that problem-solving processes involve the reorganization of cognitive maps based on new information. Second, it is demonstrated that the cognitive representation of a problem space is acquired as the animal locomotes between various points in that space. Locomotion is adduced to be the factor that provides directionality between loci in the problem space. Finally, electrophysiological data from the hippocampus are reviewed to determine the role of hippocampal activity in the mapping and problem-solving process. It is shown that hippocampal electrical activity reflected an animal's position and movement through space, These phenomena may provide potential mechanisms for cognitive mapping. However, there is no direct evidence to indicate that such electrophysiological phenomena are essential to the problemsolving process.
In recent years, the concept of a cognitive map has been receiving increasing attention both in the animal learning literature (Hulse, Fowler, & Honig, 1978) and in the neuropsychological literature (O'Keefe & Nadel, 1978). A number of properties have been attributed to a cognitive map (see O'Keefe & Nadel, 1978, pp. 89, 100), yet a mere cataloging of these properties does not reveal how such maps function in the problem-solving process, nor does it enable one to clarify the nature of the problem-solving process. By problem solving, we are referring to those behavioral integrations that appear without there having been any prior performance of the adaptive behavior (i.e., novel solutions). In contrast to problem solving, there are those behavioral integrations that reflect the association of contiguous experiences and in which the desired or correct behavior has been previously expressed (i.e., learned behaviors). Problem solving thus refers to a cognitive function of a qualitatively different nature than that implied by learning, because problem solving depends on the spontaneous integration of elements of memorial repThe contributions of E. M. Parko and C. Wages are gratefully acknowledged. 402 0163-1047/81/120402-17502.00/0 Copyright © 1981 by Academic Press, Inc. All rights of reproduction in any form reserved.
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resentations from previous isolated experiences, whereas learned behaviors are either responses to an extant cue or the expression of previously practiced behavior patterns triggered by an appropriate motivational state. A cognitive map is a memorial representation of an organism's experiences and consists of both spatial and nonspatial information. Since such maps represent not only the objects of experience but also the relationships between such objects, a variety of possible connections between the various representations of experience is present in the map. It is this latter map feature that confers to behavior a degree of flexibility greater than that which would occur were behavior merely controlled by external cues or taxes (i.e., guidances or orientations). It would therefore appear that cognitive maps should play some role in the problemsolving process, because the occurrence of novel solutions is one of the outcomes of this process. There has been an increasing number of studies attempting to demonstrate the role of the limbic forebrain in the formation of cognitive maps. More specifically, O'Keefe and Nadel (1978) have presented a major theory that defines how the hippocampus might function in the formation of such a map. They have buttressed their theoretical speculations with behavioral data indicating the effects on such map formation of lesions to various parts of the brain, particularly the hippocampus and septal area. According to O'Keefe and Nadel (1978), locomotor exploratory behavior is an important factor in the learning about places. They suggest that places are formed in the map as the animal locomotes between two points in the environment. Locomotion-induced hippocampal theta activity presumably codes the distances and directions between places into the cognitive map. In contrast to this view, Maier (1932a) noted that locomotor activity merely gives rise to successive experiences. If two points in space can only be spatially related to each other when they exist as a simultaneous pattern in experience, as suggested by Luria (1966) and Maier (1932a), then what are the circumstances whereby the successive experiences resulting from locomotor activity become simultaneous patterns? Accordingly, this paper has several purposes. The first is to demonstrate the role of cognitive maps in the problem-solving process and to indicate how the appearance of novel solutions to problems critically depends on the presence of a preexisting cognitive map. The second purpose is to examine the specific role of locomotor behavior in the formation of the cognitive map. Third, we intend to review those electrophysiological properties of the hippocampus to determine their contributions to the problem-solving process.
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Cognitive Maps and Problem Solving A major property of cognitive maps is that maps allow animals to react to stimuli that are not immediately present (i.e., "act at a distance"). An animal can use such "missing stimuli" because the relationship between those stimuli and those that are actually present in the immediate environment is represented in the cognitive map. As a result, behavior is generally more flexible than the mere execution of successive S-R sequences or orientations (i.e., turn left, turn right, etc.) or the following of specific cues (guidances). However, the mere fact of the existence of a cognitive representation of the environment does not ensure that the representation will enable a novel adaptive solution to come to expression when a previously learned behavior is no longer effective. There is nothing intrinsic in a cognitive map that selects from the many possibilities represented in the map, the one that will actually be expressed in behavior. Moreover, to the extent that a novel solution is expressed, it could not have existed in the map because the elements in the map (memorial representations) are the products of experience, and a novel solution is not a product of experience. Thus, it would appear that a novel solution to a problem would represent no! the selection of a preexisting cognitive representation of a solution but, rather, a new synthesis of specific elements of previous representations. This implies that when a novel solution occurs, there has been a combination of elements of cognitive representations, each of which was laid down independently of the other (i.e., isolated experiences). Because cognitive maps contain the memorial representations of experiences, each of which can be organized in different ways at different times, it follows that the existence of cognitive maps is a necessary but not sufficient condition for the appearance of novel solutions in problem-solving situations. What are the necessary ingredients of a task that would qualify that task as involving a problem-solving process? One approach to this question has been to emphasize the nature of the strategy that an animal follows in performing on a task. If an animal followed a cue such as a light, then that task would not be considered as involving a problemsolving function. Similarly, the presence of a multimodal stimulus in a task (e.g., spatiality) is not evidence that the task involves a problemsolving function. Olton (1979) has emphasized the "inherent ability" (p. 594) of rats to follow spatial strategies and suggested that tasks should be designed to utilize this spatial ability. He has also emphasized the role of a transfer test to determine whether performance in a task is based on a spatial or nonspatial strategy. According to Olton (1979), a transfer test is one in which a previously correct choice is no longer adaptive and a new correct response is re-
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quired. This involves traversing a route not previously used and not cued by specific extant stimuli. From the perspective of this paper, the critical aspect of the transfer test is not that it demonstrates the use of a spatial or other type of strategy but that it provides an opportunity whereby the animal's cognitive representations (maps) must become reorganized when confronted with the problem. The type of behavior displayed on the transfer test reveals the nature of the cognitive reorganization that occurred when the animal was confronted with the problem. This notion was first suggested by Maier and Schneirla (1935, p. 469). It is of particular importance to note that in maze studies where short-cut abilities were tested, there was no correlation between the ability to take a short cut (i.e., reorganize past experience based on new data) and the ability to learn the maze (Maier & Schneirla, 1935). This fact reinforces the distinction made earlier between behavioral integrations based on learned sequences and those based on cognitive restructuring. Unfortunately, there are relatively few reports in the published literature describing tasks that tap into this aspect of cognitive map function. Instead, most tasks have focused on the role of maps in spatial behavior. Although maps are involved in spatial behavior, it is our position that the spatial character of behavior is not the critical factor. Rather, the important question is the extent to which a map containing spatial representations can allow or provide for the appearance of novel solutions to spatial problems. A procedure that illustrates the function of a cognitive map in spatial problem solving involves the three-table reasoning problem originally described by Maier (1932b). In this task, animals are allowed to explore three unbaited tables and the runways connecting the tables. Following the exploration phase, the animals are fed on one of the tables (goal table). They are then placed on one of the two remaining tables (start table), and their task is to go directly from the start table to the goal table in order to receive additional food. Each day the start and goal tables are varied in a quasi-random fashion to preclude the animal's learning a specific route, table, or pattern of responding. Thus, each day's solution represents the spontaneous combination of elements of the exploratory experience with the feeding experience. Moreover, since the start table and the goal table are varied each day, the correct response each day reflects a novel solution to that day's problem. Thus, the issue of whether the animal is using a response or a spatial strategy is irrelevant. Strategies are relevant only when the correct response or choice remains constant from trial to trial. Successful performance on this task each day requires the reorganization of past experience based on new information. To the extent that the animal performs successfully, it is clear that it is using some aspect of the spatial relationships that exist among the tables.
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Behavioral observations strongly support the view that performance on this task involves the use of a maplike representation. Using the three-table task, Stahl and Ellen (1974) demonstrated that animals merely fed on one of the tables and then placed on another table to start, did not go directly to the baited table on the test trial. Animals lacking the prior exploratory experience performed at chance levels 2 on this task even if the testing procedure was continued for 18 days. As soon as the animals were given the exploratory phase prior to feeding, however, their performance on the test trial immediately attained the levels manifested by animals that always received the exploratory phase preceding the feeding phase. The feeding experience is also a crucial aspect of this procedure. It is the means whereby a table (i.e., a specific locus in space) is given motivational significance. Thus, a specific place in the cognitive map is made more salient than other places in the map. When the feeding phase is not preceded by exploration of the apparatus, the feeding experience does not allow a particular table to become salient relative to the rest of the apparatus. Thus, the feeding imparts more than simply motivational impetus. Feeding provides place information that can then be combined with other information in the map to allow for novel solutions to come to expression. In support of this analysis, Herrmann, Doherty, and Ellen (Note 1) found that if the feeding phase was given to the animals prior to the exploratory phase, the animals failed to perform above chance levels. Only when the feeding phase was given after the exploratory phase were above chance levels of performance possible on this problem.
Is Locomotion Necessary for the Formation of a Cognitive Map? This question was raised nearly 40 years ago by Thorndike in an examination of the Tolmanian concept of expectancy (Tolman, 1948). Thorndike suggested a method to test the question: "put the rat in a little wire car, in the entrance of a maze, run it through the path of a simple maze and into the food compartment. Release it there and let it eat the morsel provided. Repeat l0 to 100 times according to the difficulty of the maze under ordinary conditions. The rat had an opportunity to form expectancies that presence in the food compartment is followed by food, that the correct turn is followed by the food chamber, and so on. Then put it in the entrance chamber free to go wherever (sic) it is " B e c a u s e there is a 50% chance of being correct on any given trial, there m u s t be s o m e criterion by which performance on this task is evaluated. This is accomplished by using the e x p a n s i o n o f the binomial equation to determine the chance likelihood of a given n u m b e r of correct r e s p o n s e s in so m a n y test trials. For example, it can be determined from the e x p a n d e d binomial equation that when 20 test trials are used, the chance likelihood of being correct on 15 or more of these trials is less than 5% (p < .05). Performance below this level is considered chance performance.
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inclined and observe what it does. Compare the behavior of such rats with that of rats run in the customary manner" (Thorndike, 1946, p. 278). In an attempt to closely follow Thorndike's recommended procedure, McNamara, Long, and Wike (1956) transported rats in a basket over the runways of a T maze and then tested the animals in an extinction procedure in which the animals were placed at the start stem of the maze. The number of correct choices during nonreinforced trials did not differ between rats that were transported during acquisition training and those given conventional running experience in the maze during the acquisition period. In a second experiment in which the external room illumination was considerably reduced, the animals that were passively transported during the acquisition phase showed faster extinction of correct responding than those allowed to run during acquisition. Apparently, the salience of extramaze cues is a factor that determines the effectiveness of passive transport in the learning about places. When extramaze cues are salient, then passive transport is an effective procedure. Gleitman (1955) similarly showed that, in the absence of locomotion, rats can learn about places in the environment. In his study, rats were drawn from one place in a roon to another in a transparent cable car while receiving continuous shock. When subsequently tested on an elevated maze, where they had to choose between running to the place where shock began and where it terminated or to a neutral place, the animals showed a distinct preference for running into the place where shock was terminated. Thus, it would appear that rats can learn about the significance of places without having to locomote between these places. These passive transport experiments do not indicate, however, whether such learning extends to the relationships that exist between various locations in space. Specifically, can an animal learn the spatial relations that exist between different loci in an environment (i.e., A is to the left of B) simply by being transported between them? Some recent work by Menzel (1973, 1978) bears on this issue. He reported that chimpanzees carried around in an outdoor field in which they lived and shown a number of randomly placed hidden foods could remember the hiding place and kind of food at each place. The animals, upon being allowed to retrieve the hidden foods, generally ran directly to a food place rather than either retracing the route over which they had been carried or the reverse route. Even more important, the chimpanzees did not need to be carried along during the hiding of the food. As long as they could see the places where the food was hidden by the experimenter, they would unerringly find it. The animals ran to those places where food was located and not to those where there was no food. This experiment bears many similarities to the three-table task. First, the area in which the food was
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hidden was the chimpanzees' home area and thus had been thoroughly explored prior to the beginning of the study. The hiding of the food in different places in the field functioned to give motivational significance to some places in the field, much as the feeding experience in the threetable task gives motivational significance to one of the tables. The work of Beritoff (1965) and Ungher and Sirian (1971) has similarly shown that passive transport of an animal to a feeding locus is sufficient for that location to acquire a motivational significance for the animal. Beritoff found that if a blindfolded dog was carried in its cage to a particular area of a room, fed there, and brought back to the starting point via the same route, the animal, when released and allowed to move freely, would retrace the path to the food. The animal could retrace the path either with its eyes open or blindfolded. Control procedures eliminated the possibility that this feat was accomplished by olfactory cues or kinesthetic stimulation of the extremities. Even more complex behaviors were demonstrated in this context. If a blindfolded animal was first carried to a corner of the room where it was fed and then to another corner in the room where it was not fed, the animal, after being released several minutes later, would go directly to the corner where it was fed but not to the other corner. Placing an obstacle in front of the blindfolded animal during testing caused the animal to lose its orientation. However, if the blindfold was removed, the animal could run directly to the food location regardless of the obstacle. Finally, if a blindfolded animal was taken first to the left for a certain distance without being fed and then to the right where it was fed, it would, upon being released but still blindfolded, go directly to the place where it was fed and not along the path used by the experimenter. Although it is clear in the Menzel study that the chimpanzees had been thoroughly familiar with the field prior to having the food hidden, it is not as clear in the Befitoff studies as to whether the dogs had a prior familiarity with the experimental room. If this were indeed the case, then it could not be argued that the animals learned the spatial relations between the starting point and the feeding locus in the absence of locomotion. It is thus evident that the question whether active locomotion is necessary in the learning of spatial relations is still unanswered. A series of experiments in our laboratory was directed at this issue. In these studies, a cage was used to transport rats over the apparatus during the exploratory phase of the three-table problem. This cage consisted of a wire basket that could be pushed along the runways. The animals were given access to the tables by the experimenter opening the cage door when it was brought up to the entrance to the table. Following the usual feeding experience on one of the tables after a passive transport exploratory phase, the animals failed to solve the problem on the test trial. While this finding would seem to indicate that locomotion is nec-
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essary in the learning of the spatial relations that exist among the tables, there is a major methodological concern that mitigates against this conclusion. Inasmuch as several animals were transported over the runways in the cage together, there is a possibility that the animals were primarily engaged in exploring each other rather than orienting to the intra- and extramaze cues. Thus, it remains to be established whether an animal can indeed learn about spatial relations in the absence of locomotion. Despite the failure of our passively transported rats to perform successfully on the three-table task, their performance was such as to allow us to conclude that the procedure of passively transporting the animals was not innocuous (without consequence). The animals that were passively transported attempted to solve the problem on the test trial, as evidenced by their leaving the start table on the test trial following the feeding experience. The animals made errors of commission (Stahl & Ellen, 1973) in that they ran to the incorrect table just as often as they did to the baited table. This behavior stands in contrast to that of animals tested following the feeding phase but with no prior exploratory experience on the three-table apparatus. These latter animals also failed to solve the problem but, unlike the passively transported animals, typically refused to run on the test trials. Thus, in the absence of any exploratory phase, animals tend to make errors of omission in contrast to errors of commission. To the extent that our passively transported animals attempted to solve the three-table problem (commission errors), it would seem that these animals acquired some sort of cognitive representation of the three tables. It should be recalled that, following the transport back and forth along the runways, these animals were given access to the tables. It is possible that such access to the tables was sufficient to provide a cognitive representation of the tables such that problem-solving behavior was initiated on the test trial, but it was not sufficient to indicate to the animals how the tables were spatially related to each other. The question therefore arises as to whether exploring just the tables alone or just the runways alone would be sufficient to allow for successful problem solving to occur. To answer this question, Ellen et al. (Note 2) tested two groups of rats exposed to different exploratory conditions during the exploration phase of the three-table task. One group received access to the runways only during this phase (RO group), while the other group was only allowed to explore the tables during this phase (TO group). The latter group was exposed to a table for 5 min, then carried to another table for another 5 min exposure, and finally carried to the third table for the last 5 min of the 15-min exploratory phase. Following the standard feeding experience on one of the tables after the exploratory phase, the animals were tested in the usual manner. The results are presented in Table 1. None of the animals in the RO group and the TO
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ELLEN AND ANSCHEL TABLE 1 Effects of Type of Exploratory Experience on Three-Table Task Performance
Group
Greater than 73% correct
Less than 73% correct
Average omission errors/ 15 trials
Control RO TO
6 0 0
2 12 4
0.25 3.50 0.25
group performed above chance levels. The kinds of errors the two groups made are particularly instructive. Initially, the RO group made errors of omission which gradually decreased while errors of commission appeared. In contrast, the TO group made only errors of commission. The TO animals behaved similarly to the passively transported animals in our earlier experiments. Our passively transported animals, while failing to solve the task, made errors of commission throughout the course of testing. This fact indicates that these animals (TO group and passively transported group) acquired some cognitive representation of the tables (i.e., that the tables were connected to each other) during their exploratory phase. However, the animals apparently did not learn the spatial relationship of one table to another (e.g., table A is to the left of B). In contrast to these animals, the RO group apparently learned nothing about the tables during the exploration of the runways. They did not even learn that the tables were connected, despite running along the runways that led to the tables. Only with continued testing did their errors of omission change to errors of commission, suggesting that as they gradually ventured out from the start table on the test trial, they began to acquire information about the relationships of the tables. These findings with the RO group further indicate that running or locomotion by itself is insufficient to ensure that the animal acquires information about its environment. In order to learn that a place " A " in the environment is connected to a place " B , " the animal must both experience place A and B and then traverse the space between A and B. The results obtained with the passive transport and the TO group indicate that places in space can be connected to each other in the absence of locomotion. That problem-solving behavior is initiated on the test trial indicates that the animals have a cognitive representation of the tables. However, because they make errors of commission (go to the wrong table), it is apparent that the directionality and distance between such places in space is not part of that cognitive representation. Apparently, this kind of information is acquired only as the animal locomotes between different places in space. It would appear therefore that our behavioral findings are at least consistent with a major premise
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in the O'Keefe-Nadel theory. This conclusion posits a quite specific role for locomotion in cognitive map formation. Locomotion between places in space allows the distances and directionality between such places to be coded into the cognitive representation. We have indicated that animals must locomote back and forth between two places in space for these places to become spatially related to each other in a cognitive representation. By being spatially related, we mean simply that these places exist as simultaneous patterns in which the distance and the direction between them are specified in the cognitive representation. To the extent that place A comes after place B, then these places are simply related in a successive pattern and no spatial relationship emerges. In short, spatial relationships depend on the existence of simultaneous patterns in a cognitive representation. Thus, if two places or stimuli are perceived as a simultaneous pattern, then the animal " k n o w s " the position of the one relative to the other. If, however, the two places are perceived as successive events, then knowledge of one does not ensure that knowledge of the other exists in a specific relationship to the first. More specifically, an animal might learn that A is to the right of B without ever learning that B is to the left of A. To the extent that locomotion only provides successive experiences, how can simultaneous patterns emerge from such an experience? Maier (1932a) performed probably the only published experiment that bears directly on this issue. Three tables were placed in a triangular arrangement with interconnecting runways. Rats were trained to run from X to Y for food, from Y to Z for food, and finally from Z to X for food. This training resulted in the animals' running in a counterclockwise direction around the three tables. Following this training, the animals were given food on X and placed on Y. The question was whether the animals would run to X via the long, counterclockwise route upon which they had been trained, or would they take the short, direct, clockwise route which they had never before experienced? It was hypothesized that if the three tables were perceived as a simultaneous pattern in the rats' experience, then the animals would choose the shorter, direct route. If, however, the training only created a successive pattern of tables in the rats' experience, then the animals would select the long, counterclockwise route. They all ran the long, counterclockwise route to the food. This finding is quite important since it clearly demonstrates that when a rat runs from one place in space to another (A to B), it learns a successive association (i.e., B follows A). The rat does not necessarily learn that A is spatially related to B. In order to learn that relationship, the aninal must also run from B to A. Of further interest in this connection were the observations that a rat could run the third leg of the triangular arrangement of tables in a direction in which it had never been trained, provided that it had received
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training in both directions on the other two legs of the triangular arrangement of the tables. This finding indicates that a rat can use a successive relationship as if it were a simultaneous one provided the successive relationship is part of a pattern that is thoroughly familiar to the animal. Furthermore, this observation indicates that elements of previously established representations can be combined with current experience in order to allow the novel response to come to expression.
Electrophysiological Characteristics of Hippocampal Neuronal Activity Properties of hippocampal cells. According to the O'Keefe-Nadel theory of cognitive map formation, "psychological space" is constructed as an animal explores its environment. Exploratory behavior is activated when there is a discrepancy between the perceived environment and a previously acquired representation of that environment. Certain hippocampal cells, named misplace units, fire when an animal engages in exploratory activities in a place field either because the animal fails to find something in that field that it had been trained to find there or it discovers something new in that field (O'Keefe, 1979). As the animal explores its environment and moves from one place to another, the neuronal activity representing the multisensory stimulation arising from a given place enters the hippocampus via the entorhinal cortex to be combined into a place representation. Each place representation is coded by the firing of place cells in the hippocampus. A place cell does not respond to any particular sensory input but, rather, "constructs the notion of a place in an environment by connecting several multisensory inputs each of which can be perceived when the animal is in a particular part of an environment" (O'Keefe, 1979, p. 425). This process is reflected by a change in the firing rate when the animal is in a particular location irrespective of its behavior, specific cues, or specific experiences in the location. The entorhinal input to the hippocampus projects topographically to a narrow strip of dentate granule cells, which project in turn to a narrow strip of CA3 pyramidal cells. The CA3 axons project to a narrow strip of CA1 dendrites. Strips of these CA1 dendrites are connected into lamellae which form the basic intrahippocampal units. According to the theory, the sinusoidal hippocampal theta rhythm which enters the hippocampus via the brainstem-medial septal pathway synchronizes large areas of the hippocampus by changing the moment-tomoment excitability of hippocampal pyramidal and dentate granule cells. Hippocampal theta rhythm in the rat is maximal when the animal engages in locomotor or other voluntary behaviors and presumably carries movement information (Vanderwolf, 1969, 1971). In addition to being concomitant to voluntary behavior in the rat, hippocampal theta rhythm has a unique property, Wishaw and Vanderwolf (1973), Black (1975), and Morris, Black, and O'Keefe (1976) have
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shown that hippocampal theta frequency may be related to the distance an animal's movement translates it through the environment. This fact led to the hypothesis that hippocampal theta rhythm may sort the entorhinal inputs into different lamellae of the hippocampus as a function of the distance that the animal moves in space. The theta modulation of hippocampal cells could thus provide a mechanism for connecting the various place representations, i.e., place cell activity, into a unified representation, such as a cognitive map. Recent work by Winson and Abzug (1978) provides a clue as to the possible circuitry involved in the theta gating mechanism. They demonstrated that the transmission of action potentials through the hippocampus elicited by stimulation of the angular bundle is affected by the behavioral state of the animal. Such action potentials recorded from dentate granular and CA3 neurons were maximal in amplitude during slow-wave sleep and minimal during the still, alert condition. The potentials were intermediate in amplitude and showed considerable variability during theta states (concomitant with REM sleep and active locomotion). The possibility exists that the excitability changes observed in hippocampal neurons during theta states may be the result of modulation by the intrinsically generated theta activity. Thus, the variability of information transmission via the hippocampal pathway from dentate to CA1 may be controlled by the theta mechanism. There are a number of features of place cell activity that bear special mention. First, place cells that are adjacent to each other in the hippocampus may not have adjacent environmental place fields. Thus, unlike primary visual or auditory cortex, the hippocampal map of an environment may not be spatially isomorphic with the physical world. O'Keefe and Conway (1978) and Hill (1978) have further shown that neither body movements nor reward are significant in defining the environmental factors of place fields. Place cells appear to respond to multisensory cues irrespective of reinforcement contingencies (motivation of the animal) or the direction that an animal must turn in a T maze to obtain reward. Perhaps more importantly, place fields do not seem to be determined by any one sensery cue. Hill (1978) showed that despite the elimination of sensory modalities by surgical intervention, the same distribution of place cells were still found. The important cues signifying location for these place cells are not obvious at the moment. According to O'Keefe (1979), place cells may be reactive either to distant room cues or proximal apparatus cues. In fact, O'Keefe (1976) reports that when the apparatus is rotated, the place cell fields may be temporarily switched fron proximal to distal cues or vice versa. In this connection, Hill (1978) reported that 10 of 12 hippocampal units displayed spatial properties on the first passage of a rat through a T maze. This finding would imply that a place cell inherently responds to
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a particular spatial locus. However, the problem is not as straightforward as it would appear, since Hill's animals received considerable preoperative experience in shuttling back and forth between a pedal manipulandum and a pellet trough in the apparatus. Certainly, this prior training must have played some role in the early appearance of these place units when the animals were actually tested in the T maze. It is also noteworthy that the shuttling back and forth that Hill reported consists of a bidirectional locomotion, a factor that we have already noted as being critical for the emergence of spatiality. Thus, it would appear that Hill's findings lend support to our view that place cells acquire their unique properties by virtue of the animal's bidirectional locomotion through the environment. O'Keefe and Nadel (1978) and O'Keefe (1979) have elegantly elaborated the properties of the various types of hippocampal cells and have developed the hypothesis that these cells participate in a cognitive-mapping function. O'Keefe has suggested that if place cells constitute only a small fraction of hippocampal neurons, then the hippocampus probably has a more global function than cognitive mapping. Conversely, if a majority of hippocampal cells are place cells, it would seem that this function is basic and intrinsic to the hippocampus. Reviewing most of the studies that report Complex spike cells (58% of all hippocampal cells recorded), O'Keefe (1979) reported that 95% of the complex spike cells were place cells. Because place cells constitute the majority of hippocampal cells, it is likely that a mapping function is a significant aspect of hippocampal activity. However, if this place cell is to be part of a cognitive map, its activity must be related not only to a single place field but to other place fields which have been associated by training techniques to its place field. This implies that a place cell is conditionable in the sense that the field that activates it can be extended in space. To answer this, it is first necessary to determine whether hippocampal cells are conditionable. Hippocampal unit activity concomitant with conditioning. Electrophysiological evidence indicates that the firing pattern of neurons in the septohippocampal complex are modifiable by conditioning procedures. The classically conditioned nictitating membrane response (NMR) in the rabbit (Gormezano, 1972) has been used to reveal the effect of altering the temporal relationship between the onset of a conditioned stimulus (CS) and the onset of an unconditioned stimulus (UCS) on the unit activity recorded from CA1 and CA3 cells in the hippocampus. With paired stimuli presentation, cells in these areas increased their firing rates prior to the onset of the UCS. This increased firing rate persisted throughout the duration of the NMR and mirrored the amplitude and duration characteristics of the behavioral responses (Berger, Clark, & Thompson, 1980; Thompson, Berger, Berry, Hoehler, Rettner, & Weisz, 1980). The conditioned response of hippocampal cells required a number of paired
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C S - U C S presentations before it became manifest, but preceded the overt NMR. When the CS and UCS were not explicitly paired, there was no increase in unit activity during presentation of either CS or UCS. This finding clearly points to the effects of a conditioning procedure on the firing rate of hippocampal neurons. Neurons of the auditory pathway which are implicated in mediating the CS show different characteristics. Thompson et al. (1980) reported that in a threshold study using NMR as the behavioral indicator of detection, neurons in the cochlear nucleus, inferior colliculus, and medial geniculate nucleus show a firing pattern totally dependent on the characteristics of the auditory stimulus and unrelated to behavioral detection. Hippocampal neurons, however, showed an increased firing rate only when there was detection of the auditory stimulus as indicated by the occurrence of an NMR. This finding points to the fact that hippocampal neurons are not simply responding to the characteristics of the stimuli. Rather, the firing activity of such neurons is controlled by the temporal contingencies existing between stimuli. These results are of the utmost significance in that they demonstrate that the firing patterns of hippocampal neurons can be modified by the relationships that exist between stimuli. Thompson et al. (1980) clearly demonstrated that the range of stimuli capable of exciting hippocampal neurons can be extended via conditioning procedures. Because the hippocampus appears to be important in the processing of successive events (i.e., the temporal relationship between the CS and UCS), the possibility exists that the successive perceptions of two places in space that occur as an animal locomotes through that space can be related to each other as a simultaneous pattern in experience. We have already noted that spatial relationships depend on the existence of simultaneous patterns in a cognitive representation. It would thus follow that hippocampal neurons acquire their place properties by virtue of their conditionability. Therefore, place is a derivative of the conditionability of hippocampal neurons. This, of course, remains to be established. Discussion
We have examined three bodies of data pertaining to the formation and role of cognitive maps in spatial problem solving. The behavioral research clearly demonstrates the importance of such cognitive maps to the process. Such maps are formed as the animal explores its environment and are the means by which places in that environment are identified. Additionally, bidirectional locomotor activity between places in the environment was adduced to be the necessary condition whereby the direction and distances between the different places become encoded into the cognitive representation. Perhaps more importantly, however, spatial problem solving was shown to involve more than merely the presence
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of a cognitive map. Rather, it was suggested that problem solving involved the reorganization of past experiences based upon current information. This reorganization or integration of experience is the basic mechanism underlying the problem-solving process. Thus, a cognitive map functions as an information structure that can be dynamically altered as new information comes in. It is this dynamic alteration of the cognitive structure that leads to the appearance of novel solutions in problemsolving tasks. The third body of data examined was derived from the electrophysiological literature and demonstrated two important facets of hippocampal unit activity. First, hippocampal units could be activated when an animal was in a particular location in the environment and were presumed to correspond to the hippocampal representation of particular places in the environment. Misplace cells are activated when an animal encounters something different from what it was trained to expect at a particular location. The fact that the hippocampal unit activity reflected the amplitude and duration characteristics of the conditioned response indicated quite dramatically the lability and plasticity of hippocampal neuronal activity. Perhaps more importantly, these findings demonstrate that the range of stimuli potentially capable of activating hippocampal neurons is modifiable or extendable by associative (conditioning) procedures. A major problem still remains. While the electrophysiological data indicate that the hippocampus possesses properties and mechanisms that may function in the capacity of a map-making system, the demonstrable changes in place cell activity with changes in the position of the animal in the environment and the changes in theta frequency with movement are not equivalent to demonstrating that these changes are involved in the problem-solving process as we have outlined it. These are only potential mechanisms for such a function. In fact, it has not even been demonstrated that the problem-solving process requires such physiological mechanisms. Our analysis of the problem-solving mechanisms involved in the three-table task performance and the short-circuiting behavior in a maze indicated that such tasks create the circumstances whereby the correct behavior is based on a "brain-built knowledge" (Thomas & Brito, 1980, p. 808) which results from the spontaneous reorganization of the memorial representations occurring under the pressure of a problem situation. Whether such "brain-built knowledge" can be signaled by the firing patterns of hippocampal cells remains to be established. REFERENCES Berger, T. W., Clark, G. A., & Thompson, R. F. (1980). Learning-dependent neuronal responses recorded from limbic system brain structures during classical conditioning. Physiological Psychology, 8, 155-167. Beritoff (Beritashvili), J. S. (1965). Neural Mechanisms of Higher Vertebrate Behavior. W. T. Liberson (Ed. and Transl.). Boston: Little, Brown.
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Black, A. H. (1975). Hippocampal electrical activity and behavior. In R. L. Isaacson & K. H. Pribram (Eds.), The Hippocampus. Vol. II, New York: Plenum. Gleitman, H. (1955). Place learning without prior performance. Journal of Comparative and Physiological Psychology, 48, 77-79. Gormezano, I. (1972). Investigations of defense and reward conditioning in the rabbit. In A. H. Black & W. F. Prokasy (Eds.), Classical Conditioning 11: Current Research and Theory. New York: Appleton-Century-Crofts. Hill, A. J. (1978). First occurrence of hippocampal spatial firing in a new environment. Experimental Neurology, 62, 282-297. Hulse, S. H., Fowler, H., & Honig, W. K. (1978). Cognitive Processes in AnimalBehavior. Hillsdale, N.J.: Erlbaum. Luria, A. R. (1966). Human Brain and Psychological Processes. New York: Harper & Row. Maier, N. R. F. (1932). A study of orientation in the rat. Journal of Comparative Psychology, 14, 387-399. (a) Maier, N. R. F. (1932). Cortical destruction of the posterior part of the brain and its effects on reasoning in rats. Journal of Comparative Neurology, 56, 179-214. (b) Maier, N. R. F., & Schneirla, T. C. (1935). Principles of Animal Psychology. New York: McGraw-Hill. McNamara, H. J., Long, J. B., & Wike, E. L. (1956). Learning without response under two conditions of external cues. Journal of Comparative and Physiological Psychology, 49, 477-480. Menzel, E. (1973). Chimpanzee spatial memory organization. Science, 182, 943-945. Menzel, E. (1978). Cognitive mapping in chimpanzees. In S. H. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive Processes in Animal Behavior. Hillsdale, N.J.: Erlbaum. Morris, R. G. M., Black, A. H., & O'Keefe, J. (1976). Hippocampal EEG during a ballistic movement. Neurosciences Letters, 3, 102 (Abstract). O'Keefe, J. (1976). Place units in the hippocampus of the freely moving rat. Experimental Neurology, 51, 78-109. O'Keefe, J. (1979). A review of the hippocampal place cells. Progress in Neurobiology, 13, 419-439. O'Keefe, J., & Conway, D. H. (1978). Hippocampal place units in the freely moving rat: Why they fire where they fire. Experimental Brain Research, 31, 537-590. O'Keefe, J., & Nadel, L. (1978). The Hippocampus as a Cognitive Map. London/New York: Oxford Univ. Press (Clarendon). Olton, D. S. (1979). Mazes, maps and memory. American Psychologist, 34, 583-596. Stahl, J., & Ellen, P. (1973). Septal lesions and reasoning performance in the rat. Journal of Comparative and Physiological Psychology, 84, 629-638. Stahl, J., & Ellen, P. (1974). Factors in the reasoning performance of the rat. Journal of Comparative and Physiological Psychology, 87, 598-604. Thomas, G. J., & Brito, G. N. O. (1980). Recovery of delayed alternation in rats after lesions in medial frontal cortex and septum. Journal of Comparative and Physiological Psychology, 94, 808-818. Thompson, R. F., Berger, T. W., Berry, S. D., Hoehler, F. K., Rettner, R. E., & Weisz, D. J. (1980). Hippocampal substrate of classical conditioning. Physiological Psychology, 8, 262-279. Thorndike, E. L. (1946). Expectation. Psychological Review, 53, 277-281. Tolman, E. C. (1948). Cognitive maps in man and animals. Psychological Review, 55, 189-208. Ungher, J., & Sirian S. (1971). Vestibular short-term memory deficits due to behavior disturbances induced by fornix lesions in cat. Review of Roumanian Neurology, 8, 407-417.
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Vanderwolf, C. H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalography and Clinical Neurophysiology, 26, 407-418. Vanderwolf, C. H. (1971). Limbic-diencephalic mechanisms of voluntary movement. Psychological Review, 78, 83-113. Winson, J., & Abzug, C. (1978). Neuronal transmission through hippocampal pathways dependent on behavior. Journal of Neurophysiology, 4, 716-732. Wishaw, I. Q., & Vanderwolf, C. H. (1973). Hippocampal EEG and behavior: Changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behavioral Biology, 8, 461-484.
REFERENCE NOTES 1. Herrmann, T., Doherty, D., & Ellen, P. Places vs routes in spatial problem solving. Unpublished manuscript. 2. Ellen, P., Wages, C., & Parko, E. M. Cognitive maps in bits and pieces. Unpublished nanuscript.
33, 402-418 (1981)
Problem Solving in the Rat: Cognitive/Physiological Mechanisms 1 PAUL ELLEN AND STEVEN ANSCHEL
Department of Psychology, Georgia State University, Atlanta, Georgia 30303 Three bodies of data pertaining to the role of cognitive maps in animal problem solving are examined. First, it is shown that problem-solving processes involve the reorganization of cognitive maps based on new information. Second, it is demonstrated that the cognitive representation of a problem space is acquired as the animal locomotes between various points in that space. Locomotion is adduced to be the factor that provides directionality between loci in the problem space. Finally, electrophysiological data from the hippocampus are reviewed to determine the role of hippocampal activity in the mapping and problem-solving process. It is shown that hippocampal electrical activity reflected an animal's position and movement through space, These phenomena may provide potential mechanisms for cognitive mapping. However, there is no direct evidence to indicate that such electrophysiological phenomena are essential to the problemsolving process.
In recent years, the concept of a cognitive map has been receiving increasing attention both in the animal learning literature (Hulse, Fowler, & Honig, 1978) and in the neuropsychological literature (O'Keefe & Nadel, 1978). A number of properties have been attributed to a cognitive map (see O'Keefe & Nadel, 1978, pp. 89, 100), yet a mere cataloging of these properties does not reveal how such maps function in the problem-solving process, nor does it enable one to clarify the nature of the problem-solving process. By problem solving, we are referring to those behavioral integrations that appear without there having been any prior performance of the adaptive behavior (i.e., novel solutions). In contrast to problem solving, there are those behavioral integrations that reflect the association of contiguous experiences and in which the desired or correct behavior has been previously expressed (i.e., learned behaviors). Problem solving thus refers to a cognitive function of a qualitatively different nature than that implied by learning, because problem solving depends on the spontaneous integration of elements of memorial repThe contributions of E. M. Parko and C. Wages are gratefully acknowledged. 402 0163-1047/81/120402-17502.00/0 Copyright © 1981 by Academic Press, Inc. All rights of reproduction in any form reserved.
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resentations from previous isolated experiences, whereas learned behaviors are either responses to an extant cue or the expression of previously practiced behavior patterns triggered by an appropriate motivational state. A cognitive map is a memorial representation of an organism's experiences and consists of both spatial and nonspatial information. Since such maps represent not only the objects of experience but also the relationships between such objects, a variety of possible connections between the various representations of experience is present in the map. It is this latter map feature that confers to behavior a degree of flexibility greater than that which would occur were behavior merely controlled by external cues or taxes (i.e., guidances or orientations). It would therefore appear that cognitive maps should play some role in the problemsolving process, because the occurrence of novel solutions is one of the outcomes of this process. There has been an increasing number of studies attempting to demonstrate the role of the limbic forebrain in the formation of cognitive maps. More specifically, O'Keefe and Nadel (1978) have presented a major theory that defines how the hippocampus might function in the formation of such a map. They have buttressed their theoretical speculations with behavioral data indicating the effects on such map formation of lesions to various parts of the brain, particularly the hippocampus and septal area. According to O'Keefe and Nadel (1978), locomotor exploratory behavior is an important factor in the learning about places. They suggest that places are formed in the map as the animal locomotes between two points in the environment. Locomotion-induced hippocampal theta activity presumably codes the distances and directions between places into the cognitive map. In contrast to this view, Maier (1932a) noted that locomotor activity merely gives rise to successive experiences. If two points in space can only be spatially related to each other when they exist as a simultaneous pattern in experience, as suggested by Luria (1966) and Maier (1932a), then what are the circumstances whereby the successive experiences resulting from locomotor activity become simultaneous patterns? Accordingly, this paper has several purposes. The first is to demonstrate the role of cognitive maps in the problem-solving process and to indicate how the appearance of novel solutions to problems critically depends on the presence of a preexisting cognitive map. The second purpose is to examine the specific role of locomotor behavior in the formation of the cognitive map. Third, we intend to review those electrophysiological properties of the hippocampus to determine their contributions to the problem-solving process.
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Cognitive Maps and Problem Solving A major property of cognitive maps is that maps allow animals to react to stimuli that are not immediately present (i.e., "act at a distance"). An animal can use such "missing stimuli" because the relationship between those stimuli and those that are actually present in the immediate environment is represented in the cognitive map. As a result, behavior is generally more flexible than the mere execution of successive S-R sequences or orientations (i.e., turn left, turn right, etc.) or the following of specific cues (guidances). However, the mere fact of the existence of a cognitive representation of the environment does not ensure that the representation will enable a novel adaptive solution to come to expression when a previously learned behavior is no longer effective. There is nothing intrinsic in a cognitive map that selects from the many possibilities represented in the map, the one that will actually be expressed in behavior. Moreover, to the extent that a novel solution is expressed, it could not have existed in the map because the elements in the map (memorial representations) are the products of experience, and a novel solution is not a product of experience. Thus, it would appear that a novel solution to a problem would represent no! the selection of a preexisting cognitive representation of a solution but, rather, a new synthesis of specific elements of previous representations. This implies that when a novel solution occurs, there has been a combination of elements of cognitive representations, each of which was laid down independently of the other (i.e., isolated experiences). Because cognitive maps contain the memorial representations of experiences, each of which can be organized in different ways at different times, it follows that the existence of cognitive maps is a necessary but not sufficient condition for the appearance of novel solutions in problem-solving situations. What are the necessary ingredients of a task that would qualify that task as involving a problem-solving process? One approach to this question has been to emphasize the nature of the strategy that an animal follows in performing on a task. If an animal followed a cue such as a light, then that task would not be considered as involving a problemsolving function. Similarly, the presence of a multimodal stimulus in a task (e.g., spatiality) is not evidence that the task involves a problemsolving function. Olton (1979) has emphasized the "inherent ability" (p. 594) of rats to follow spatial strategies and suggested that tasks should be designed to utilize this spatial ability. He has also emphasized the role of a transfer test to determine whether performance in a task is based on a spatial or nonspatial strategy. According to Olton (1979), a transfer test is one in which a previously correct choice is no longer adaptive and a new correct response is re-
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quired. This involves traversing a route not previously used and not cued by specific extant stimuli. From the perspective of this paper, the critical aspect of the transfer test is not that it demonstrates the use of a spatial or other type of strategy but that it provides an opportunity whereby the animal's cognitive representations (maps) must become reorganized when confronted with the problem. The type of behavior displayed on the transfer test reveals the nature of the cognitive reorganization that occurred when the animal was confronted with the problem. This notion was first suggested by Maier and Schneirla (1935, p. 469). It is of particular importance to note that in maze studies where short-cut abilities were tested, there was no correlation between the ability to take a short cut (i.e., reorganize past experience based on new data) and the ability to learn the maze (Maier & Schneirla, 1935). This fact reinforces the distinction made earlier between behavioral integrations based on learned sequences and those based on cognitive restructuring. Unfortunately, there are relatively few reports in the published literature describing tasks that tap into this aspect of cognitive map function. Instead, most tasks have focused on the role of maps in spatial behavior. Although maps are involved in spatial behavior, it is our position that the spatial character of behavior is not the critical factor. Rather, the important question is the extent to which a map containing spatial representations can allow or provide for the appearance of novel solutions to spatial problems. A procedure that illustrates the function of a cognitive map in spatial problem solving involves the three-table reasoning problem originally described by Maier (1932b). In this task, animals are allowed to explore three unbaited tables and the runways connecting the tables. Following the exploration phase, the animals are fed on one of the tables (goal table). They are then placed on one of the two remaining tables (start table), and their task is to go directly from the start table to the goal table in order to receive additional food. Each day the start and goal tables are varied in a quasi-random fashion to preclude the animal's learning a specific route, table, or pattern of responding. Thus, each day's solution represents the spontaneous combination of elements of the exploratory experience with the feeding experience. Moreover, since the start table and the goal table are varied each day, the correct response each day reflects a novel solution to that day's problem. Thus, the issue of whether the animal is using a response or a spatial strategy is irrelevant. Strategies are relevant only when the correct response or choice remains constant from trial to trial. Successful performance on this task each day requires the reorganization of past experience based on new information. To the extent that the animal performs successfully, it is clear that it is using some aspect of the spatial relationships that exist among the tables.
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Behavioral observations strongly support the view that performance on this task involves the use of a maplike representation. Using the three-table task, Stahl and Ellen (1974) demonstrated that animals merely fed on one of the tables and then placed on another table to start, did not go directly to the baited table on the test trial. Animals lacking the prior exploratory experience performed at chance levels 2 on this task even if the testing procedure was continued for 18 days. As soon as the animals were given the exploratory phase prior to feeding, however, their performance on the test trial immediately attained the levels manifested by animals that always received the exploratory phase preceding the feeding phase. The feeding experience is also a crucial aspect of this procedure. It is the means whereby a table (i.e., a specific locus in space) is given motivational significance. Thus, a specific place in the cognitive map is made more salient than other places in the map. When the feeding phase is not preceded by exploration of the apparatus, the feeding experience does not allow a particular table to become salient relative to the rest of the apparatus. Thus, the feeding imparts more than simply motivational impetus. Feeding provides place information that can then be combined with other information in the map to allow for novel solutions to come to expression. In support of this analysis, Herrmann, Doherty, and Ellen (Note 1) found that if the feeding phase was given to the animals prior to the exploratory phase, the animals failed to perform above chance levels. Only when the feeding phase was given after the exploratory phase were above chance levels of performance possible on this problem.
Is Locomotion Necessary for the Formation of a Cognitive Map? This question was raised nearly 40 years ago by Thorndike in an examination of the Tolmanian concept of expectancy (Tolman, 1948). Thorndike suggested a method to test the question: "put the rat in a little wire car, in the entrance of a maze, run it through the path of a simple maze and into the food compartment. Release it there and let it eat the morsel provided. Repeat l0 to 100 times according to the difficulty of the maze under ordinary conditions. The rat had an opportunity to form expectancies that presence in the food compartment is followed by food, that the correct turn is followed by the food chamber, and so on. Then put it in the entrance chamber free to go wherever (sic) it is " B e c a u s e there is a 50% chance of being correct on any given trial, there m u s t be s o m e criterion by which performance on this task is evaluated. This is accomplished by using the e x p a n s i o n o f the binomial equation to determine the chance likelihood of a given n u m b e r of correct r e s p o n s e s in so m a n y test trials. For example, it can be determined from the e x p a n d e d binomial equation that when 20 test trials are used, the chance likelihood of being correct on 15 or more of these trials is less than 5% (p < .05). Performance below this level is considered chance performance.
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inclined and observe what it does. Compare the behavior of such rats with that of rats run in the customary manner" (Thorndike, 1946, p. 278). In an attempt to closely follow Thorndike's recommended procedure, McNamara, Long, and Wike (1956) transported rats in a basket over the runways of a T maze and then tested the animals in an extinction procedure in which the animals were placed at the start stem of the maze. The number of correct choices during nonreinforced trials did not differ between rats that were transported during acquisition training and those given conventional running experience in the maze during the acquisition period. In a second experiment in which the external room illumination was considerably reduced, the animals that were passively transported during the acquisition phase showed faster extinction of correct responding than those allowed to run during acquisition. Apparently, the salience of extramaze cues is a factor that determines the effectiveness of passive transport in the learning about places. When extramaze cues are salient, then passive transport is an effective procedure. Gleitman (1955) similarly showed that, in the absence of locomotion, rats can learn about places in the environment. In his study, rats were drawn from one place in a roon to another in a transparent cable car while receiving continuous shock. When subsequently tested on an elevated maze, where they had to choose between running to the place where shock began and where it terminated or to a neutral place, the animals showed a distinct preference for running into the place where shock was terminated. Thus, it would appear that rats can learn about the significance of places without having to locomote between these places. These passive transport experiments do not indicate, however, whether such learning extends to the relationships that exist between various locations in space. Specifically, can an animal learn the spatial relations that exist between different loci in an environment (i.e., A is to the left of B) simply by being transported between them? Some recent work by Menzel (1973, 1978) bears on this issue. He reported that chimpanzees carried around in an outdoor field in which they lived and shown a number of randomly placed hidden foods could remember the hiding place and kind of food at each place. The animals, upon being allowed to retrieve the hidden foods, generally ran directly to a food place rather than either retracing the route over which they had been carried or the reverse route. Even more important, the chimpanzees did not need to be carried along during the hiding of the food. As long as they could see the places where the food was hidden by the experimenter, they would unerringly find it. The animals ran to those places where food was located and not to those where there was no food. This experiment bears many similarities to the three-table task. First, the area in which the food was
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hidden was the chimpanzees' home area and thus had been thoroughly explored prior to the beginning of the study. The hiding of the food in different places in the field functioned to give motivational significance to some places in the field, much as the feeding experience in the threetable task gives motivational significance to one of the tables. The work of Beritoff (1965) and Ungher and Sirian (1971) has similarly shown that passive transport of an animal to a feeding locus is sufficient for that location to acquire a motivational significance for the animal. Beritoff found that if a blindfolded dog was carried in its cage to a particular area of a room, fed there, and brought back to the starting point via the same route, the animal, when released and allowed to move freely, would retrace the path to the food. The animal could retrace the path either with its eyes open or blindfolded. Control procedures eliminated the possibility that this feat was accomplished by olfactory cues or kinesthetic stimulation of the extremities. Even more complex behaviors were demonstrated in this context. If a blindfolded animal was first carried to a corner of the room where it was fed and then to another corner in the room where it was not fed, the animal, after being released several minutes later, would go directly to the corner where it was fed but not to the other corner. Placing an obstacle in front of the blindfolded animal during testing caused the animal to lose its orientation. However, if the blindfold was removed, the animal could run directly to the food location regardless of the obstacle. Finally, if a blindfolded animal was taken first to the left for a certain distance without being fed and then to the right where it was fed, it would, upon being released but still blindfolded, go directly to the place where it was fed and not along the path used by the experimenter. Although it is clear in the Menzel study that the chimpanzees had been thoroughly familiar with the field prior to having the food hidden, it is not as clear in the Befitoff studies as to whether the dogs had a prior familiarity with the experimental room. If this were indeed the case, then it could not be argued that the animals learned the spatial relations between the starting point and the feeding locus in the absence of locomotion. It is thus evident that the question whether active locomotion is necessary in the learning of spatial relations is still unanswered. A series of experiments in our laboratory was directed at this issue. In these studies, a cage was used to transport rats over the apparatus during the exploratory phase of the three-table problem. This cage consisted of a wire basket that could be pushed along the runways. The animals were given access to the tables by the experimenter opening the cage door when it was brought up to the entrance to the table. Following the usual feeding experience on one of the tables after a passive transport exploratory phase, the animals failed to solve the problem on the test trial. While this finding would seem to indicate that locomotion is nec-
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essary in the learning of the spatial relations that exist among the tables, there is a major methodological concern that mitigates against this conclusion. Inasmuch as several animals were transported over the runways in the cage together, there is a possibility that the animals were primarily engaged in exploring each other rather than orienting to the intra- and extramaze cues. Thus, it remains to be established whether an animal can indeed learn about spatial relations in the absence of locomotion. Despite the failure of our passively transported rats to perform successfully on the three-table task, their performance was such as to allow us to conclude that the procedure of passively transporting the animals was not innocuous (without consequence). The animals that were passively transported attempted to solve the problem on the test trial, as evidenced by their leaving the start table on the test trial following the feeding experience. The animals made errors of commission (Stahl & Ellen, 1973) in that they ran to the incorrect table just as often as they did to the baited table. This behavior stands in contrast to that of animals tested following the feeding phase but with no prior exploratory experience on the three-table apparatus. These latter animals also failed to solve the problem but, unlike the passively transported animals, typically refused to run on the test trials. Thus, in the absence of any exploratory phase, animals tend to make errors of omission in contrast to errors of commission. To the extent that our passively transported animals attempted to solve the three-table problem (commission errors), it would seem that these animals acquired some sort of cognitive representation of the three tables. It should be recalled that, following the transport back and forth along the runways, these animals were given access to the tables. It is possible that such access to the tables was sufficient to provide a cognitive representation of the tables such that problem-solving behavior was initiated on the test trial, but it was not sufficient to indicate to the animals how the tables were spatially related to each other. The question therefore arises as to whether exploring just the tables alone or just the runways alone would be sufficient to allow for successful problem solving to occur. To answer this question, Ellen et al. (Note 2) tested two groups of rats exposed to different exploratory conditions during the exploration phase of the three-table task. One group received access to the runways only during this phase (RO group), while the other group was only allowed to explore the tables during this phase (TO group). The latter group was exposed to a table for 5 min, then carried to another table for another 5 min exposure, and finally carried to the third table for the last 5 min of the 15-min exploratory phase. Following the standard feeding experience on one of the tables after the exploratory phase, the animals were tested in the usual manner. The results are presented in Table 1. None of the animals in the RO group and the TO
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ELLEN AND ANSCHEL TABLE 1 Effects of Type of Exploratory Experience on Three-Table Task Performance
Group
Greater than 73% correct
Less than 73% correct
Average omission errors/ 15 trials
Control RO TO
6 0 0
2 12 4
0.25 3.50 0.25
group performed above chance levels. The kinds of errors the two groups made are particularly instructive. Initially, the RO group made errors of omission which gradually decreased while errors of commission appeared. In contrast, the TO group made only errors of commission. The TO animals behaved similarly to the passively transported animals in our earlier experiments. Our passively transported animals, while failing to solve the task, made errors of commission throughout the course of testing. This fact indicates that these animals (TO group and passively transported group) acquired some cognitive representation of the tables (i.e., that the tables were connected to each other) during their exploratory phase. However, the animals apparently did not learn the spatial relationship of one table to another (e.g., table A is to the left of B). In contrast to these animals, the RO group apparently learned nothing about the tables during the exploration of the runways. They did not even learn that the tables were connected, despite running along the runways that led to the tables. Only with continued testing did their errors of omission change to errors of commission, suggesting that as they gradually ventured out from the start table on the test trial, they began to acquire information about the relationships of the tables. These findings with the RO group further indicate that running or locomotion by itself is insufficient to ensure that the animal acquires information about its environment. In order to learn that a place " A " in the environment is connected to a place " B , " the animal must both experience place A and B and then traverse the space between A and B. The results obtained with the passive transport and the TO group indicate that places in space can be connected to each other in the absence of locomotion. That problem-solving behavior is initiated on the test trial indicates that the animals have a cognitive representation of the tables. However, because they make errors of commission (go to the wrong table), it is apparent that the directionality and distance between such places in space is not part of that cognitive representation. Apparently, this kind of information is acquired only as the animal locomotes between different places in space. It would appear therefore that our behavioral findings are at least consistent with a major premise
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in the O'Keefe-Nadel theory. This conclusion posits a quite specific role for locomotion in cognitive map formation. Locomotion between places in space allows the distances and directionality between such places to be coded into the cognitive representation. We have indicated that animals must locomote back and forth between two places in space for these places to become spatially related to each other in a cognitive representation. By being spatially related, we mean simply that these places exist as simultaneous patterns in which the distance and the direction between them are specified in the cognitive representation. To the extent that place A comes after place B, then these places are simply related in a successive pattern and no spatial relationship emerges. In short, spatial relationships depend on the existence of simultaneous patterns in a cognitive representation. Thus, if two places or stimuli are perceived as a simultaneous pattern, then the animal " k n o w s " the position of the one relative to the other. If, however, the two places are perceived as successive events, then knowledge of one does not ensure that knowledge of the other exists in a specific relationship to the first. More specifically, an animal might learn that A is to the right of B without ever learning that B is to the left of A. To the extent that locomotion only provides successive experiences, how can simultaneous patterns emerge from such an experience? Maier (1932a) performed probably the only published experiment that bears directly on this issue. Three tables were placed in a triangular arrangement with interconnecting runways. Rats were trained to run from X to Y for food, from Y to Z for food, and finally from Z to X for food. This training resulted in the animals' running in a counterclockwise direction around the three tables. Following this training, the animals were given food on X and placed on Y. The question was whether the animals would run to X via the long, counterclockwise route upon which they had been trained, or would they take the short, direct, clockwise route which they had never before experienced? It was hypothesized that if the three tables were perceived as a simultaneous pattern in the rats' experience, then the animals would choose the shorter, direct route. If, however, the training only created a successive pattern of tables in the rats' experience, then the animals would select the long, counterclockwise route. They all ran the long, counterclockwise route to the food. This finding is quite important since it clearly demonstrates that when a rat runs from one place in space to another (A to B), it learns a successive association (i.e., B follows A). The rat does not necessarily learn that A is spatially related to B. In order to learn that relationship, the aninal must also run from B to A. Of further interest in this connection were the observations that a rat could run the third leg of the triangular arrangement of tables in a direction in which it had never been trained, provided that it had received
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training in both directions on the other two legs of the triangular arrangement of the tables. This finding indicates that a rat can use a successive relationship as if it were a simultaneous one provided the successive relationship is part of a pattern that is thoroughly familiar to the animal. Furthermore, this observation indicates that elements of previously established representations can be combined with current experience in order to allow the novel response to come to expression.
Electrophysiological Characteristics of Hippocampal Neuronal Activity Properties of hippocampal cells. According to the O'Keefe-Nadel theory of cognitive map formation, "psychological space" is constructed as an animal explores its environment. Exploratory behavior is activated when there is a discrepancy between the perceived environment and a previously acquired representation of that environment. Certain hippocampal cells, named misplace units, fire when an animal engages in exploratory activities in a place field either because the animal fails to find something in that field that it had been trained to find there or it discovers something new in that field (O'Keefe, 1979). As the animal explores its environment and moves from one place to another, the neuronal activity representing the multisensory stimulation arising from a given place enters the hippocampus via the entorhinal cortex to be combined into a place representation. Each place representation is coded by the firing of place cells in the hippocampus. A place cell does not respond to any particular sensory input but, rather, "constructs the notion of a place in an environment by connecting several multisensory inputs each of which can be perceived when the animal is in a particular part of an environment" (O'Keefe, 1979, p. 425). This process is reflected by a change in the firing rate when the animal is in a particular location irrespective of its behavior, specific cues, or specific experiences in the location. The entorhinal input to the hippocampus projects topographically to a narrow strip of dentate granule cells, which project in turn to a narrow strip of CA3 pyramidal cells. The CA3 axons project to a narrow strip of CA1 dendrites. Strips of these CA1 dendrites are connected into lamellae which form the basic intrahippocampal units. According to the theory, the sinusoidal hippocampal theta rhythm which enters the hippocampus via the brainstem-medial septal pathway synchronizes large areas of the hippocampus by changing the moment-tomoment excitability of hippocampal pyramidal and dentate granule cells. Hippocampal theta rhythm in the rat is maximal when the animal engages in locomotor or other voluntary behaviors and presumably carries movement information (Vanderwolf, 1969, 1971). In addition to being concomitant to voluntary behavior in the rat, hippocampal theta rhythm has a unique property, Wishaw and Vanderwolf (1973), Black (1975), and Morris, Black, and O'Keefe (1976) have
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shown that hippocampal theta frequency may be related to the distance an animal's movement translates it through the environment. This fact led to the hypothesis that hippocampal theta rhythm may sort the entorhinal inputs into different lamellae of the hippocampus as a function of the distance that the animal moves in space. The theta modulation of hippocampal cells could thus provide a mechanism for connecting the various place representations, i.e., place cell activity, into a unified representation, such as a cognitive map. Recent work by Winson and Abzug (1978) provides a clue as to the possible circuitry involved in the theta gating mechanism. They demonstrated that the transmission of action potentials through the hippocampus elicited by stimulation of the angular bundle is affected by the behavioral state of the animal. Such action potentials recorded from dentate granular and CA3 neurons were maximal in amplitude during slow-wave sleep and minimal during the still, alert condition. The potentials were intermediate in amplitude and showed considerable variability during theta states (concomitant with REM sleep and active locomotion). The possibility exists that the excitability changes observed in hippocampal neurons during theta states may be the result of modulation by the intrinsically generated theta activity. Thus, the variability of information transmission via the hippocampal pathway from dentate to CA1 may be controlled by the theta mechanism. There are a number of features of place cell activity that bear special mention. First, place cells that are adjacent to each other in the hippocampus may not have adjacent environmental place fields. Thus, unlike primary visual or auditory cortex, the hippocampal map of an environment may not be spatially isomorphic with the physical world. O'Keefe and Conway (1978) and Hill (1978) have further shown that neither body movements nor reward are significant in defining the environmental factors of place fields. Place cells appear to respond to multisensory cues irrespective of reinforcement contingencies (motivation of the animal) or the direction that an animal must turn in a T maze to obtain reward. Perhaps more importantly, place fields do not seem to be determined by any one sensery cue. Hill (1978) showed that despite the elimination of sensory modalities by surgical intervention, the same distribution of place cells were still found. The important cues signifying location for these place cells are not obvious at the moment. According to O'Keefe (1979), place cells may be reactive either to distant room cues or proximal apparatus cues. In fact, O'Keefe (1976) reports that when the apparatus is rotated, the place cell fields may be temporarily switched fron proximal to distal cues or vice versa. In this connection, Hill (1978) reported that 10 of 12 hippocampal units displayed spatial properties on the first passage of a rat through a T maze. This finding would imply that a place cell inherently responds to
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a particular spatial locus. However, the problem is not as straightforward as it would appear, since Hill's animals received considerable preoperative experience in shuttling back and forth between a pedal manipulandum and a pellet trough in the apparatus. Certainly, this prior training must have played some role in the early appearance of these place units when the animals were actually tested in the T maze. It is also noteworthy that the shuttling back and forth that Hill reported consists of a bidirectional locomotion, a factor that we have already noted as being critical for the emergence of spatiality. Thus, it would appear that Hill's findings lend support to our view that place cells acquire their unique properties by virtue of the animal's bidirectional locomotion through the environment. O'Keefe and Nadel (1978) and O'Keefe (1979) have elegantly elaborated the properties of the various types of hippocampal cells and have developed the hypothesis that these cells participate in a cognitive-mapping function. O'Keefe has suggested that if place cells constitute only a small fraction of hippocampal neurons, then the hippocampus probably has a more global function than cognitive mapping. Conversely, if a majority of hippocampal cells are place cells, it would seem that this function is basic and intrinsic to the hippocampus. Reviewing most of the studies that report Complex spike cells (58% of all hippocampal cells recorded), O'Keefe (1979) reported that 95% of the complex spike cells were place cells. Because place cells constitute the majority of hippocampal cells, it is likely that a mapping function is a significant aspect of hippocampal activity. However, if this place cell is to be part of a cognitive map, its activity must be related not only to a single place field but to other place fields which have been associated by training techniques to its place field. This implies that a place cell is conditionable in the sense that the field that activates it can be extended in space. To answer this, it is first necessary to determine whether hippocampal cells are conditionable. Hippocampal unit activity concomitant with conditioning. Electrophysiological evidence indicates that the firing pattern of neurons in the septohippocampal complex are modifiable by conditioning procedures. The classically conditioned nictitating membrane response (NMR) in the rabbit (Gormezano, 1972) has been used to reveal the effect of altering the temporal relationship between the onset of a conditioned stimulus (CS) and the onset of an unconditioned stimulus (UCS) on the unit activity recorded from CA1 and CA3 cells in the hippocampus. With paired stimuli presentation, cells in these areas increased their firing rates prior to the onset of the UCS. This increased firing rate persisted throughout the duration of the NMR and mirrored the amplitude and duration characteristics of the behavioral responses (Berger, Clark, & Thompson, 1980; Thompson, Berger, Berry, Hoehler, Rettner, & Weisz, 1980). The conditioned response of hippocampal cells required a number of paired
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C S - U C S presentations before it became manifest, but preceded the overt NMR. When the CS and UCS were not explicitly paired, there was no increase in unit activity during presentation of either CS or UCS. This finding clearly points to the effects of a conditioning procedure on the firing rate of hippocampal neurons. Neurons of the auditory pathway which are implicated in mediating the CS show different characteristics. Thompson et al. (1980) reported that in a threshold study using NMR as the behavioral indicator of detection, neurons in the cochlear nucleus, inferior colliculus, and medial geniculate nucleus show a firing pattern totally dependent on the characteristics of the auditory stimulus and unrelated to behavioral detection. Hippocampal neurons, however, showed an increased firing rate only when there was detection of the auditory stimulus as indicated by the occurrence of an NMR. This finding points to the fact that hippocampal neurons are not simply responding to the characteristics of the stimuli. Rather, the firing activity of such neurons is controlled by the temporal contingencies existing between stimuli. These results are of the utmost significance in that they demonstrate that the firing patterns of hippocampal neurons can be modified by the relationships that exist between stimuli. Thompson et al. (1980) clearly demonstrated that the range of stimuli capable of exciting hippocampal neurons can be extended via conditioning procedures. Because the hippocampus appears to be important in the processing of successive events (i.e., the temporal relationship between the CS and UCS), the possibility exists that the successive perceptions of two places in space that occur as an animal locomotes through that space can be related to each other as a simultaneous pattern in experience. We have already noted that spatial relationships depend on the existence of simultaneous patterns in a cognitive representation. It would thus follow that hippocampal neurons acquire their place properties by virtue of their conditionability. Therefore, place is a derivative of the conditionability of hippocampal neurons. This, of course, remains to be established. Discussion
We have examined three bodies of data pertaining to the formation and role of cognitive maps in spatial problem solving. The behavioral research clearly demonstrates the importance of such cognitive maps to the process. Such maps are formed as the animal explores its environment and are the means by which places in that environment are identified. Additionally, bidirectional locomotor activity between places in the environment was adduced to be the necessary condition whereby the direction and distances between the different places become encoded into the cognitive representation. Perhaps more importantly, however, spatial problem solving was shown to involve more than merely the presence
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of a cognitive map. Rather, it was suggested that problem solving involved the reorganization of past experiences based upon current information. This reorganization or integration of experience is the basic mechanism underlying the problem-solving process. Thus, a cognitive map functions as an information structure that can be dynamically altered as new information comes in. It is this dynamic alteration of the cognitive structure that leads to the appearance of novel solutions in problemsolving tasks. The third body of data examined was derived from the electrophysiological literature and demonstrated two important facets of hippocampal unit activity. First, hippocampal units could be activated when an animal was in a particular location in the environment and were presumed to correspond to the hippocampal representation of particular places in the environment. Misplace cells are activated when an animal encounters something different from what it was trained to expect at a particular location. The fact that the hippocampal unit activity reflected the amplitude and duration characteristics of the conditioned response indicated quite dramatically the lability and plasticity of hippocampal neuronal activity. Perhaps more importantly, these findings demonstrate that the range of stimuli potentially capable of activating hippocampal neurons is modifiable or extendable by associative (conditioning) procedures. A major problem still remains. While the electrophysiological data indicate that the hippocampus possesses properties and mechanisms that may function in the capacity of a map-making system, the demonstrable changes in place cell activity with changes in the position of the animal in the environment and the changes in theta frequency with movement are not equivalent to demonstrating that these changes are involved in the problem-solving process as we have outlined it. These are only potential mechanisms for such a function. In fact, it has not even been demonstrated that the problem-solving process requires such physiological mechanisms. Our analysis of the problem-solving mechanisms involved in the three-table task performance and the short-circuiting behavior in a maze indicated that such tasks create the circumstances whereby the correct behavior is based on a "brain-built knowledge" (Thomas & Brito, 1980, p. 808) which results from the spontaneous reorganization of the memorial representations occurring under the pressure of a problem situation. Whether such "brain-built knowledge" can be signaled by the firing patterns of hippocampal cells remains to be established. REFERENCES Berger, T. W., Clark, G. A., & Thompson, R. F. (1980). Learning-dependent neuronal responses recorded from limbic system brain structures during classical conditioning. Physiological Psychology, 8, 155-167. Beritoff (Beritashvili), J. S. (1965). Neural Mechanisms of Higher Vertebrate Behavior. W. T. Liberson (Ed. and Transl.). Boston: Little, Brown.
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Vanderwolf, C. H. (1969). Hippocampal electrical activity and voluntary movement in the rat. Electroencephalography and Clinical Neurophysiology, 26, 407-418. Vanderwolf, C. H. (1971). Limbic-diencephalic mechanisms of voluntary movement. Psychological Review, 78, 83-113. Winson, J., & Abzug, C. (1978). Neuronal transmission through hippocampal pathways dependent on behavior. Journal of Neurophysiology, 4, 716-732. Wishaw, I. Q., & Vanderwolf, C. H. (1973). Hippocampal EEG and behavior: Changes in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats. Behavioral Biology, 8, 461-484.
REFERENCE NOTES 1. Herrmann, T., Doherty, D., & Ellen, P. Places vs routes in spatial problem solving. Unpublished manuscript. 2. Ellen, P., Wages, C., & Parko, E. M. Cognitive maps in bits and pieces. Unpublished nanuscript.