O'Keefe and Nadel (1978) distinguish two paradigms for navigation, the "locale system" for map-based navigation and the "taxon (behavioral orientation) system" for route navigation. This article models the taxon system, the map-based system, and their interaction, and argues that the map-based system involves the interaction of hippocampus and other systems.
We relate taxes to the notion of an affordance. Just as a rat may have basic taxes for approaching food or avoiding a bright light, so does it have a wider repertoire of affordances for possible actions associated with immediate sensing of its environment. We propose that affordances are extracted by the rat posterior parietal cortex, which guides action selection by the premotor cortex and is influenced also by hypothalamic drive information.
The taxon-affordances model (TAM) for taxon-based determination of movement direction is based on models of frog detour behavior, with expectations of future reward implemented using reinforcement learning. The specification of the direction of movement is refined by current affordances and motivational information to yield an appropriate course of action.
The world graph (WG) theory expands the idea of a map by developing the hypothesis that cognitive and motivational states interact. This article describes an implementation of this theory, the WG model. The integrated TAM-WG model then allows us to explain data on the behavior of rats with and without fornix lesions, which disconnect the hippocampus from other neural systems.
Apicella, P., Scarnati, E., Ljungberg, T., & Schultz, W. (1992). Neuronal activity in monkey striatum related to the expectation of predictable environmental events. Journal of Neurophysiology, 68(3), 945-960.
2.
Arbib, M.A. (1972). The metaphorical brain: Cybernetics as artificial intelligence and brain theory. New York: Wiley-Interscience.
3.
Arbib, M.A. (1997). From visual affordances in monkey parietal cortex to hippocampo-parietal interactions underlying rat navigation. Philosophical Transactions of the Royal Society (London )B, 352(1360), 1429-1436.
4.
Arbib, M.A., Érdi, P., & Szentágothai, J. (1997). Neural organization: Structure, function, and dynamics. Cambridge, MA: Bradford Books/MIT Press.
5.
Arbib, M.A., & House, D.H. (1987). Depth and detours: An essay on visually guided behavior. In M. A. Arbib & A. R. Hanson (Eds.), Vision, brain and cooperative computation. Cambridge, MA: Bradford Books/MIT Press.
6.
Arbib, M.A., & Lieblich, I. (1977). Motivational learning of spatial behavior. In J. Metzler (Eds.), Systems neuroscience . New York: Academic.
7.
Barto, A.G. (1995). Adaptive critics and the basal ganglia. In J. C. Houk et al. (Eds.), Models of information processing in the basal ganglia. Cambridge, MA: MIT Press.
8.
Barto, A.G., Richard, S., & Anderson, C.W. (1983). Neuronlike adaptive elements that can solve difficult learning control problems. IEEE Transactions on Systems, Man, and Cybernetics, SMC-13, 834-846.
9.
Barto, A.G., & Sutton, R.S. (1981). Landmark learning: An illustration of associative search. Biological Cybernetics, 42, 1-8.
10.
Burgess, N., Reece, M., & O'Keefe, J. (1994). A model of hippocampal function. Neural Networks, 7, 1065-1081.
11.
Chen, L.L., Lin, L.H., Barnes, C.A., & McNaughton, B.L. (1994b). Head-direction cells in the rat posterior cortex: 2. Contributions of visual and ideothetic information to the directional firing. Experimental Brain Research , 101(1), 24-34.
12.
Chen, L.L., Lin, L.H., Green, E.J., Barnes, C.A., & McNaughton, B.L. (1994a). Head-direction cells in the rat posterior cortex: 1. Anatomical distribution and behavioral modulation. Experimental Brain Research101(1), 8-23.
13.
Collett, T. (1982). Do toads plan routes? A study of detour behavior of B. viridis. Journal of Comparative Physiology [A], 146, 261-271.
14.
Corbacho, F.J., & Arbib, M.A. (1995). Learning to detour. Adaptive Behavior3(4), 419-468.
15.
Dayan, P. (1991). Navigating through temporal difference. In R. P. Lippmann et al. (Eds.), Neural Information Processing Systems, Vol. 3. San Mateo: Morgan Kaufmann.
16.
Dominey, P.F., & Arbib, M.A. (1992). A cortico-subcortical model for generation of spatially accurate sequential saccades. Cerebral Cortex, 2, 135-175.
17.
Etienne, A.S., Maurer, R., & Seguinot, V. (1996). Path integration in mammals and its interaction with visual landmarks. Journal of Experimental Biology, 199(pt 1), 201-209.
18.
Fagg, A.H. (1996). A computational model of the cortical mechanisms involved in primate grasping. Unpublished doctoral thesis,University of Southern California.
19.
Gibson, J.J. (1966). The senses considered as perceptual systems. London: Allen and Unwin.
20.
Goodridge, J.P., & Taube, J.S. (1995). Preferential use of the landmark navigational system by head direction cells in rats. Behavioral Neuroscience , 109(1), 49-61.
21.
Hirsh, R., Leber, B., & Gillman, K. (1978). Fornix fibers and motivational states as controllers of behavior: A study stimulated by the contextual retrieval theory. Behavioral Biology, 22, 463-478.
22.
Hull, C.L. (1943). Principles of behavior. New York: Appleton-Century-Crofts.
23.
Ingle, D. (1980). The frog's detection of stationary objects following lesions of the pretectum. Behavioral Brain Research, 3, 151-173.
24.
Klopf, A.H. (1972). Brain function and adaptive systems—a heterostatic theory (Air Force Cambridge Research Laboratory Research Report No. AFCRL-72-0164) . Bedford, MA: Air Force Cambridge Research Laboratory. (A summary appears in Proceedings of the International Conference on Systems, Man, and Cybernetics , 1974.)
25.
Knierim, J.J., Kudrimoti, H.S., & McNaughton, B.L. (1995). Place cells, head direction cells, and the learning of landmark stability. Journal of Neuroscience, 15(3, pt 1), 1648-1659.
26.
Knierim, J.J., McNaughton, B.L., Duffield, C., & Bliss, J. (1993). On the binding of hippocampal place fields to the inertial orientation system. Society for Neuroscience Abstracts, 19, 795.
27.
Kolb, B., Buhrmann, K., McDonald, R., & Sutherland, R.J. (1994). Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. Cerebral Cortex4(6), 664-680.
28.
Lavoie, A.M., & Mizumori, S.J. (1994). Spatial, movement- and reward-sensitive discharge by medial ventral striatum neurons of rats. Brain Research, 638, 157-168.
29.
Lieblich, I., & Arbib, M.A. (1982). Multiple representations of space underlying behavior . The Behavioral and Brain Sciences, 5, 627-659.
30.
Markus, E.J., Barnes, C.A., McNaughton, B.L., Gladden, V.L., & Skaggs, W.E. (1994). Spatial information content and reliability of hippocampal CA1 neurons: Effects of visual input. Hippocampus , 4(4), 410-421.
31.
Markus, E.J., Qin, Y.L., Leonard, B., Skaggs, W.E., McNaughton, B.L., & Barnes, C.A. (1995). Interactions between location and task affect the spatial and directional firing of hippocampal neurons. Journal of Neuroscience, 15, 7079-7094.
32.
McNaughton, B.L., Barnes, C.A., Gerrard, J.L., Gothard, K., Jung, M.W., Knierim, J.J., Kudrimoti, H., Qin, Y., Skaggs, W.E., Suster, M., & Weaver, K.L. (1996). Deciphering the hippocampal polyglot: The hippocampus as a path integration system. Journal of Experimental Biology , 199(pt 1), 173-185.
33.
McNaughton, B.L., Barnes, C.A., & O'Keefe, J. (1983). The contributions of position, direction, and velocity to single unit activity in the hippocampus of freely-moving rats . Experimental Brain Research, 52(1), 41-49.
34.
McNaughton, B.L., Knierim, J.J., & Wilson, M.A. (1994b). Vector encoding and the vestibular foundations of spatial cognition: Neurophysiological and computational mechanisms. In M. Gazzaniga (Ed.), The cognitive neurosciences. Boston: MIT Press .
35.
McNaughton, B.L., Leonard, B., & Chen, L. (1989). Cortico-hippocampal interactions and cognitive mapping: A hypothesis based on reintegration of the parietal and inferotemporal pathways for visual processing. Psychobiology, 17, 230-235.
36.
McNaughton, B.L., Mizumori, S.J., Barnes, C.A., Leonard, B.J., Marquis, M., & Green, E.J. (1994a). Cortical representation of motion during unrestrained spatial navigation in the rat. Cerebral Cortex, 4(1), 27-39.
37.
Mirenowicz, J., & Schultz, W. (1996). Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature, 379, 449-451.
38.
Mishkin, M., Ungerleider, L.G., & Mack, K.A. (1983). Object vision and spatial vision: Two cortical pathways. Trends in Neuroscience, 6, 414-417.
39.
Mittelstaedt, M.L., & Mittelstaedt, H. (1980). Homing by path integration in a mammal. Naturwissenchaft, 67, 566-567.
40.
Morris, R.G., Garrud, P., Rawlins, J.N., & O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868), 681-683.
41.
Morris, R.G.M., Hagan, J.J., & Rawlins, J. N. P. (1986). Allocentric spatial learning by hippocampectomised rats: A further test of "spatial mapping" and "working memory" theories of hippocampal function. Quarterly Journal of Experimental Psychology, 38B, 365-395.
42.
Muller, R.U., Bostock, E., Taube, J.S., & Kubie, J.L. (1994). On the directional firing properties of hippocampal place cells. Journal of Neuroscience, 14, 7235-7251.
43.
Muller, R.U., Kubie, J.L., Bostock, E.M., Taube, J.S., & Quirk, G.J. (1991). Spatial firing correlates of neurons in the hippocampal formation of freely moving rats. In J. Paillard (Ed.), Brain and space (pp. 296-333). Oxford: Oxford University Press.
44.
Muller, R.U., Kubie, J.L., & Ranck, J.B., Jr. (1987). Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. Journal of Neuroscience, 7,1935-1950.
45.
O'Keefe, J. (1983). Spatial memory within and without the hippocampal system. In W Seifert (Ed.), Neurobiology of the hippocampusNew York: Academic.
46.
O'Keefe, J., & Burgess, N. (1996). Geometric determinants of the place fields of hippocampal neurons. Nature, 381, 425-428.
47.
O'Keefe, J., and Conway, D.H. (1980). On the trail of the hippocampal engram. Physiological Psychology, 8, 229-238.
48.
O'Keefe, J., & Dostrovsky, J. (1971). The hippocampus as a spatial map: Preliminary evidence from unit activity in the freely moving rat. Brain Research, 34, 171-175.
49.
O'Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon.
50.
Olton, D.S., Becker, J.T., & Handelmann, G.E. (1980). Hippocampal function: Working memory or cognitive mapping? Physiological Psychology , 8, 239-246.
51.
Packard, M.G., & McGaugh, J.L. (1992). Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behavioral Neuroscience, 106(3), 439-446.
52.
Poucet, B. (1993). Spatial cognitive maps in animals: New hypotheses on their structure and neural mechanisms. Psychological Review , 100(2), 163-182.
53.
Quirk, G.J., Muller, R.U., & Kubie, J.L. (1990). The firing of hippocampal place cells in the dark depends on the rat's recent experience. Journal of Neuroscience , 10(6), 2008-2017.
54.
Risold, P.Y., & Swanson, L.W. (1995). Evidence for a hypothalamo-thalamocortical circuit mediating pheromonal influences on eye and head movements. Proceedings of the National Academy of Sciences of the United States of America, 92(9), 3898-3902.
55.
Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G., & Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey II. Area F5 and the control of distal movements. Experimental Brain Research, 71, 491-507.
56.
Sakata, H., Shibutani, H., Ito, Y., Tsurugai, K., Mine, S., & Kusunoki, M. (1994). Functional properties of rotation-sensitive neurons in the posterior parietal association cortex of the monkey. Experimental Brain Research, 101(2), 183-202.
57.
Samsonovich, A. (1997). Attractor map theory of the hippocampal representation of space. Unpublished doctoral thesis, University of Arizona .
58.
Samsonovich, A., & McNaughton, B.L. (1997). Path integration and cognitive mapping in a continuous attractor neural network model. Journal of Neuroscience, 1715,5900-5920.
59.
Save, E., & Moghaddam, M. (1996). Effects of lesions of the associative parietal cortex on the acquisition and use of spatial memory in egocentric and allocentric navigation tasks in the rat. Behavioral Neuroscience, 110(1), 74-85.
60.
Schenk, F., & Morris, R.G.M. (1985). Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions. Experimental Brain Research, 58, 11-28.
61.
Schmajuk, N.A. (1990). Role of the hippocampus in temporal and spatial navigation : An adaptive neural network. Behavioral Brain Research, 39(3), 205-229.
62.
Schmajuk, N.A., & Blair, H.T. (1993). Place learning and the dynamics of spatial navigation: A neural network approach. Adaptive Behavior, 1, 355-387.
63.
Schmajuk, N.A., & Thieme, A.D. (1992). Purposive behavior and cognitive mapping : A neural network model. Biological Cybernetics, 67, 165-174.
64.
Schultz, W., Romo, R., Ljungberg, T., Mirenowicz, J., Hollerman, J.R., & Dickinson, A. (1995). Reward-related signals carried by dopamine neurons . In J. R. Houk et al. (Eds.), Models of information processing in the basal ganglia. Cambridge, MA: MIT Press.
65.
Shibata, H., & Kato, A. (1993). Topographic relationship between anteromedial thalamic nucleus neurons and their cortical terminal fields in the rat. Neuroscience Research, 17(1), 63-69.
66.
Sutherland, R.J., & Rodriguez, A.J. (1989). The role of the fornix/fimbria and some related subcortical structures in place learning and memory. Behavioral Brain Research, 32(3), 265-277.
67.
Sutton, S.S. (1988). Learning to predict by the methods of temporal differences. Machine Learning, 3, 9-44.
68.
Swanson, L.W., & Mogenson, G.J. (1981). Neural mechanisms for the functional coupling of autonomic, endocrine and somatomotor responses in adaptive behavior. Brain Research Reviews, 3, 1-34.
69.
Taube, J.S., Muller, R.U., & Ranck, J.B., Jr. (1990a). Head-direction cells recorded from the postsubiculum in freely moving rats: II. Effects of environmental manipulations. Journal of Neuroscience, 10(2), 436-447.
70.
Taube, J.S., Muller, R.U., & Ranck, J.B., Jr. (1990b). Head-direction cells recorded from the postsubiculum in freely moving rats: I. Description and quantitative analysis. Journal of Neuroscience, 10, 420-435.
71.
Taube, J.S., Jr. (1995). Head direction cells recorded in the anterior thalamic nuclei of freely moving rats. Journal of Neuroscience , 15(1, pt 1), 70-86.
72.
Thinus-Blanc, C. (1996). Animal spatial cognition: Behavioral and brain approach. Singapore : World Scientific .
73.
Toates, F. (1986). Motivational systems. Cambridge , Engl.: Cambridge University Press.
74.
Tolman, E.C. (1948). Cognitive maps in rats and men. Psychological Review, 55, 189-208.
75.
Touretzky, D.S., & Redish, A.D. (1996). Theory of rodent navigation based on interacting representations of space. Hippocampus, 6, 247-270.
76.
Wiener, S.I. (1993). Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. Journal of Neuroscience, 13(9), 3802-3817.
