HIPPOCAMPUS VOL. 2, NO. 3, PAGES 335-338, JULY 1992

Letter to the Editors Which Spatial Behavior Are We Talking About?

To the Editors: A recent issue of Hippocampus (1:221-340, 1991) presented a forum addressing the question “Is the hippocampal formation preferentially involved in spatial behavior?” Organized around a lead article in which L. Nadel summarized his views, and followed by shorter essays that gave rise to many insightful comments, the forum demonstrated the vitality of this field of research. However, most comments dealt almost exclusively with the hippocampus and memory. With a few notable exceptions, spatial behavior itself and the underlying psychological mechanisms were not discussed, despite Nadel’s emphasis on the need for a multilevcl analysis (p. 225). The analysis of psychological processes is one of these levels. Spatial memory, which refers to several forms of memory (procedural, propositional, egocentric, exocentric, etc.) but to a single domain (space) is but one of the psychological processes involved in spatial behaviors (and we use the plural intentionally here). The term spatial behaviors should by no means be reduced to memory. It is therefore difficult to respond adequately to the target question without having first defined spatial behaviors. O’Keefe and Nadel’s The Hippocampus as a Cognitive Map (1978) became the bedside book for researchers interested in space because it provided a balanced proportioning of ingredients from various sources, ranging from philosophy to brain studies. Such a comprehensive approach is not evident in the comments in response to Nadel’s lead article, which leads us to conclude that either spatial behavior has not been investigated adequately and retains its mystery, or that behavioral studies have been relegated to the background in this issue. Because we, with many other colleagues, have been primarily interested in spatial behavior for many years, we consider the second alternative more likely. We comment herein on what we believe to be an important issue and one that merits inclusion on any discussion of the relationship of spatial behavior and the underlying psychological and brain processes.

What is spatial behavior? Every observable behavior is, by its very nature, spatial. Therefore, one must clearly define the term spatial behavior. First, a distinction should be made between those spatial behaviors relying on O’Keefe and Nadel’s (1978) “taxon system” (guidances and reorientations) and those belonging to the “locale system.” The latter behaviors involve the use of maps (ix., the representation of a number of spatial relations provided by the environment). That damage to the hippocampal formation primarily affects the behaviors from this

secondary category has been well documented. The initial question, “Is the hippocampal formation preferentially involved in spatial behavior?” could therefore be reformulated to “Is the hippocampal formation preferentially involved in spatial maps?” But what is a spatial map? In recent years, several models about which spatial relations are encoded and how they are encoded have flourished. Among the most precisely stated proposals is McNaughton’s (1988) computational model, which argues that a map consists of a matrix associating specific local views with particular movements, resulting in the prediction of the next local view to be attained. As O’Keefe emphasized in the forum, this is a sophisticated form of stimulus-response associations. A second model was proposed by Collett et al. (1986) and further developed by Cheng (1989). Based on the results of welldesigned experiments, these authors suggested that the localization of an inconspicuous goal would be computed by subtracting a vector perceived by the animal when it points to that landmark from its current start location (hence a “seen” vector). This form of spatial representation, although not a map, can account for spatial navigation in the Moms water maze provided that distant landmarks are available from any place in the water maze. This questions the interpretation, in terms of survey maps, of many experiments aimed at demonstrating the existence and nature of such maps. However, although this proposal accounts for oriented displacements under some conditions, it has the major drawback of being uneconomical (Collett et al., 1986) and not allowing for flexible behaviors such as those observed in detour situations (Chapuis et al., 1983; Poucet et al., 1983). These detour experiments suggest that the spatial representation used by animals is not goal-centered (i.e., is not limited to a stored vector between a landmark and a goal), but also encompasses the structure of the possible paths between the subject’s current location and the goal. Other models, such as those proposed by O’Keefe (1990: 1991) and Muller et al. (1991), attempt to account for true spatial mapping in terms of either metric or topological relations, respectively (see also these authors’ comments in response to the lead article). From these considerations, it is clear that the term spatial behavior can refer to a wide range of underlying mechanisms, some of which hardly correspond to an actual spatial mapping. We argue, however, that an examination of the functions of spatial maps may be useful in understanding their adaptive importance. Even behaviors that might appear rather basic to some investigators may require the operation of an actual spatial mapping process for their function (see Gaffan’s essay in the forum). Our aim here is to consider one of these functions. Because the functions of spatial representations in memory, orientation, and planning are well acknowledged, we instead focus on their functions in spatial recognition and identification.

Spatial recognition and identification A spatial representation is necessary to ensure the recognition and identification of the subject’s current environment. It is well known that an organism must be familiar with its surroundings to display the elementary actions required for

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its survival (Ellen et al., 1982; Renner, 1988; 1990). As em- is only one component of the whole process resulting in spaphasized by Nadel in the lead article, exploratory activity tial behavior. Additionally, maps must be stored for further appears to fulfill this basic function. Contrary to his concern use in orientation. The several divergent opinions expressed (p. 224), however, some progress has been achieved in the in this forum show that the precise function of the hippoinsight into the functional value of exploration. Recent re- campal formation in these latter phases is still a matter for search has demonstrated that exploratory activity acts as a debate. This divergence stresses the flaws in the view that spatial builder. A host of converging data shows that most the hippocampal formation implements a cognitive map. To suggest possible answers to the target question, it may changes in the spatial arrangement of visual as well as olfactory cues, when these changes occur after habituation (i-e., be helpful to consider the roles of other brain structures, such when the animals are already familiar with the environment), as the parietal and prefrontal cortices, possibly involved at are accurately detected and located by rodents (Thinus-Blanc the various stages of the process. Since the relative develand Ingle, 1985; Thinus-Blanc et al., 1987; 1992; Poucet et opment of neocortical areas varies considerably according to al., 1986; Tomlinson and Johnston, 1991; Xavier et al., 1991). the species under consideration, it is arguable that homoloThe geometric arrangement of the objects appears to be the gous structures will be involved differently in spatial prospatial parameter preferentially encoded during exploration cesses. We therefore suggest that there are two prerequisites for answering the original target question. First, at the psy(see also Gallistel, 1990). Animals with lesions to the hippocampal formation appear chological level, one must fractionate the whole process reto be quite unable to detect such discrete topographical sulting in spatial behavior into its constituent phases to evaluchanges (Poucet, 1989; Xavier et al., 1990; Save et al., 1992a; ate the role of the hippocampal formation at each of these 1992b). These results stand in marked contrast to Suther- phases. Second, one must weigh the conclusions meeting the land’s (1985) report that hippocampal lesions do not affect first prerequisite according to the species under study. This the detection of topographic modifications (see also Suth- would provide a better insight to the likely parallel phylogeny erland and Rudy’s essay in the forum). Two likely explana- of the mental states and brain substrates. This view appears tions for this discrepancy are as follows: (1) In Sutherland’s to be more in accordance with the modern conceptions of (1985) experiment the whole arena containing the explored brain functioning that go far beyond the traditional relationobjects was rotated 180” relative to the external cues, re- ship between structures and functions. sulting in a much more important change than in the aboveBruno Poucet cited experiments, which used discrete spatial changes of the Catherine Thinus-Blanc initial configuration. (2) The time course of the pretest haCenter National de la Recherche Scientifique bituation sessions was far longer in Sutherland’s experiment Laboratoire de Neurosciences Cognitives (5 minute daily sessions for about 30 days) than in the other Marseille, France studies (usually a few sessions clustered in at most 2 days). This may have promoted the storage of spatial information in extrahippocampal structures (Kubie et al., 1989). References Additionally, further experiments dispel the hypothesis that the hippocampal deficit in reaction to a spatial change Chapuis, N., C. Thinus-Blanc, and B. Poucet (1983) Dissociation of mechanisms involved in dogs’ oriented displacements. Q . J. Exp. might result from a failure to encode spatial relations during Psychol. 35Bz213-219. the pretest exploratory phase. Indeed, it has been demonstrated that reversible inactivation of the hippocampus, when Cheng, K. (1989) The vector sum model of pigeon landmark use. J. Exp. Psychol. [Anim. Behav.] 15:366-375. produced after habituation but before the test session, also Collett, T. S., B. A. Cartwright, and B. A. Smith (1986) Landmark results in a failure to detect the change (Thinus-Blanc et al., learning and visuo-spatial memories in gerbils. J. Comp. Physiol. 1991). A158:835-851 This set of data unambiguously demonstrates that during Ellen, P., E. M. Parko, C. Wages, D. Doherty, and T. 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Finally, these results demonstrate unequivocally that tation and information storage. In Neural Connections and Mental the hippocampus plays a fundamental role in this function. Computations, L. Nadel, L. A. Cooper, P. Culicover, and R. M. I

Is the hippocampal formation preferentially involved in spatial maps? On the basis of the above considerations, a first element of response to this question is that the hippocampal formation is necessary for the building up of maps. However, this phase

Harnish, eds., pp. 285-350, MIT Press, Cambridge, MA. Muller, R. U., J. L. Kubie, E. M. Bostock, J. S. Taube, G. J. Quirk (1991) Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In Brain and Space, J. Paillard, ed., pp. 296-333, Oxford University Press, Oxford, U.K. O’Keefe, J. (1990) A computational theory of the hippocampal cognitive map. Prog. Brain Res. 83:301-312. O’Keefe, J. (1991) The hippocampal cognitive map and navigational

LETTERTOTHEEDITOR strategies. InErain and Space, J. Paillard, ed., pp. 273-295, Oxford University Press, Oxford, U.K. O’Keefe, J., and L. Nadel(1978) The Hippocampus as a Cognitive Map. Clarendon Press, Oxford. Poucet, B., N. Chapuis, M. Dump, and C. Thinus-Blanc (1986) A study of exploratory behavior as an index of spatial knowledge in hamsters. Anim. Learn. Behav. 14:93-100. Poucet, B., C. Thinus-Blanc, and N. Chapuis (1983) Route-planning in cats, in relation to the visibility of the goal. Anim. Behav. 31 594599. Poucet, B. (1989) Object exploration, habituation and response to a spatial change in rats following septa1 or medial frontal cortical damage. Behav. Neurosci. 103:1009- 1016. Renner, M. J. (1988) Learning during exploration: The role of behavioral topography during exploration in determining subsequent adaptive behavior. Int. J. Comp. Psychol. 2:43-56. Renner, M. J. (1990) Neglected aspects of exploratory and investigatory behavior. Psychobiology 18: 16-22. Save, E., M.-C. Buhot, N. Forcman, and C. Thinus-Blanc (1992a) Exploratory activity and response to a spatial change in rats with hippocampal or posterior parietal cortical lesions. Behav. Brain Res. (in press). Save, E., B. Poucet, N. Foreman, and M.-C. Buhot (1992b) Object exploration and reactions to spatial and non spatial changes in hooded rats following damage to parietal cortex or dorsal hippocampus. Behav. Neurosci. (in press). Sutherland, R. J. (1985) The navigating hippocampus: An individual

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medley of movement, space, and memory. In Electrical Activity of the Archicortex, G . Buzsaki and C. H . Vandenvolf, eds., pp. 255-279. Akademiai Kiado, Budapest. Thinus-Blanc, C., and D. Ingle (1985) Spatial behaviour in gerbils. J. Comp. Psychol. 99:311-315. Thinus-Blanc, C., L. Bouzouba, K. Chaix, N. Chapuis, M. Dump, and B. Poucet (1987) A study of spatial parameters encoded during exploration in hamsters. J. Exp. Psychol. [Anim. Behav.] 13:418427. Thinus-Blanc, C., E . Save, B. Poucet, and M.-C. Buhot (1991) The effects of reversible inactivation of hippocampus on exploratory activity and spatial memory. Hippocampus 1:363-369. Thinus-Blanc, C., M. Dump, and B. Poucet (1992) The spatial parameters encoded by hamsters during exploration: A further study. Behav. Proc. 26:43-57. Tolman, E. C. (1948) Cognitive maps in rats and men. Psychol. Rev. 55:189-208. Tomlinson, W. T., and T. D. Johnston (1991) Hamsters represent spatial information derived from olfactory cues. Anim. Learn. Behav. 19:185-190. Xavier, G. F., M. I. Porto Saito, and C. Stein (1991) Habituation of exploratory activity to new stimuli, to the absence of a previously presented stimulus and to new contexts, in rats. Q. J. Exp. Psychol. 43B: 157- 175. Xavier, G. F., C. Stein, and 0. F. A. Bueno (1990) Rats with hippocampal lesions do react to new stimuli but not to spatial changes of known stimuli. Behav. Neurol Biol. 54:172-183.

Which spatial behavior are we talking about?

HIPPOCAMPUS VOL. 2, NO. 3, PAGES 335-338, JULY 1992 Letter to the Editors Which Spatial Behavior Are We Talking About? To the Editors: A recent issu...
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