Abstract
To navigate in their environment, rodents are able to rely on a variety of behavioral strategies. The most flexible strategies result from their ability to form spatial representations that encode information about spatial cues and about important places (nest, goals, etc). In the present chapter, we address the issues of cue and place encoding in the brain brain and suggest that they are crucial processes for behavioral flexibility and adaptation to environmental changes. First, it is suggested that, due to a different spatial distribution (distant vs. nearby) or nature (allothetic allothetic vs. idiothetic) of spatial cues, animals use and have to coordinate the use of multiple spatial reference frames. This involves activation of various brain regions including the hippocampus and neocortical areas. In particular, location-specifc activity of hippocampal neurons (place cells) place cell has been shown to be controlled by different reference frames. Second, we present new data suggesting that activity of prefrontal cortex neurons reflects goal encoding. It is concluded that the knowledge of these mechanisms in animals may be a source of inspiration to improve the adaptive capacities of navigating robots.
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References
Banquet, J.-P., Gaussier, P., Quoy, M., Revel, A., Burnod, Y.: Cortico-hippocampal maps and navigation strategies in robots and rodents. In: Hallan, B., Floreano, D., Hallam, J., Hallam, B., Hages, G., Meyer, J.-A. (eds.) From animals to animats, vol. 7, pp. 141–150. MIT press, Boston (2002)
Benhamou, S., Poucet, B.: Landmark use by navigating rats (rattus norvegicus) contrasting geometric and featural information. J. Comp. Psychol. 112, 317–322 (1998)
Best, P.J., White, A.M., Minai, A.: Spatial processing in the brain: the activity of hippocampal place cells. Ann. Rev. Neurosci. 24, 459–486 (2001)
Breese, C.R., Hampson, R.E., Deadwyler, S.A.: Hippocampal place cells: stereotypy and plasticity. J. Neurosci. 9, 1097–1111 (1989)
Brown, J.E., Skaggs, W.E.: Concordant and discordant coding of spatial location in populations of hippocampal CA1 pyramidal cells. J. Neurophysiol. 88, 1605–1613 (2002)
Bureš, J., Fenton, A.A., Yu, K., Zinyuk, L.: Place cells and place navigation. Proc. Natl. Acad. Sci. 94, 343–350 (1997)
Burgess, N., O’Keefe, J.: Spatial Models of the Hippocampus. In: Arbib, M.A. (ed.) The Handbook of Brain Theory and Neural Networks, 2nd edn., pp. 468–472. MIT press, Cambridge (2002)
Burgess, N., O’Keefe, J.: Neural representations in human spatial memory. Trends Cogn. Sci. 7, 517–519 (2003)
Cardinal, R.N., Parkinson, J.A., Hall, J., Everitt, B.J.: Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321–352 (2002)
Cressant, A., Muller, R.U., Poucet, B.: Failure of centrally placed objects to control the firing fields of hippocampal place cells. J. Neurosci. 17, 2532–2542 (1997)
Cressant, A., Muller, R.U., Poucet, B.: Further study of the control of place cell firing by intra-apparatus objects. Hippocampus 9, 423–431 (1999)
Dalley, J.W., Cardinal, R.N., Robbins, T.W.: Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci. Biobehav. Rev. 28, 771–784 (2004)
Eichenbaum, H., Stewart, C., Morris, R.G.: Hippocampal representation in place learning. J. Neurosci. 10, 3531–3542 (1990)
Etienne, A.S., Jeffery, K.J.: Path integration in mammals. Hippocampus 14, 180–192 (2004)
Fenton, A.A., Stuchlik, A., Kaminsky, Y., Zahálka, A., Bureš, J.: Place avoidance by path integration is only accurate for about 7 m without useful visual and substratal cues. Soc. Neurosci. Abst. 24, 1685 (1998)
Fenton, A.A., Wesierska, M., Kaminsky, Y., Bureš, J.: Both here and there: simultaneous expression of autonomous spatial memories in rats. Proc. Natl. Acad. Sci. 95, 11493–11498 (1998)
Ferino, F., Thierry, A.M., Glowinski, J.: Anatomical and electrophysiological evidence for a direct projection from Ammon’s horn to the medial prefrontal cortex in the rat. Exp. Brain Res. 65, 421–426 (1987)
Filliat, D., Meyer, J.-A.: Map-based navigation in mobile robots. I. A review of localization strategies. J. Cog. Syst. Res. 4, 243–282 (2003)
Gaussier, P., Revel, A., Banquet, J.-P., Babeau, V.: From view cells and place cells to cognitive map learning: processing stages of the hippocampal system. Biol. Cybern. 86, 16–28 (2002)
Gothard, K.M., Skaggs, W.E., McNaughton, B.L.: Dynamics of mismatch correction in the hippocampal ensemble code for space: interaction between path integration and environmental cues. J. Neurosci. 16, 8027–8040 (1996)
Gothard, K.M., Skaggs, W.E., Moore, K.M., McNaughton, B.L.: Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci. 16, 823–835 (1996)
Gould-Beierle, K.L., Kamil, A.C.: The use of local and global cues by Clarck nutcrackers, Nucifraga Columbiana. Anim. Behav. 52, 519–528 (1996)
Hok, V., Save, E., Lenck-Santini, P.-P., Poucet, B.: Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex. Proc. Natl. Acad. Sci. 102, 4602–4607 (2005)
Hollup, S.A., Molden, S., Donnet, J.G., Moser, M.-B., Moser, E.I.: Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J. Neurosci. 21, 1635–1644 (2001)
Jeffery, K.J., O’Keefe, J.: Learned interaction of visual and idiothetic cues in the control of place field orientation. Exp. Brain Res. 127, 151–161 (1999)
Knierim, J.J.: Dynamic interactions between local surface cues, distal landmarks, and intrinsic circuitry in hippocampal place cells. J. Neurosci. 22, 6254–6264 (2002)
Knierim, J.J., Kudrimoti, H.S., McNaughton, B.L.: Interactions between idiothetic and external landmarks in the control of place cells and head direction cells. J. Neurophysiol. 80, 425–446 (1998)
Lavenex, P., Schenk, F.: Olfactory cues potentiate learning of distant visuospatial information. Neurobiol. Learn Mem. 68, 140–153 (1997)
Lenck-Santini, P.-P., Muller, R.U., Save, E., Poucet, B.: Relationships between place cell firing fields and navigational decisions by rats. J. Neurosci. 22, 9035–9047 (2002)
Lenck-Santini, P.-P., Save, E., Poucet, B.: Evidence for a relationship between place-cell spatial firing and spatial memory performance. Hippocampus 11, 377–390 (2001)
Lever, C., Wills, T., Cacucci, F., Burgess, N., O’Keefe, J.: Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90–94 (2002)
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.: Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199, 173–185 (1996)
Meyer, J.-A., Filliat, D.: Map-based navigation in mobile robots. II. A review of map-learning and path planning strategies. J. Cog. Syst. Res. 4, 283–317 (2003)
Morris, R.G.M.: Spatial localization does not require the presence of local cues. Learn Motiv. 12, 239–260 (1981)
Muller, R.U.: A quarter of a century of place cells. Neuron 17, 813–822 (1996)
Muller, R.U., Kubie, J.L.: The effects of changes in the environment on the spatial firing of hippocampal complex-spike cells. J. Neurosci. 7, 1951–1968 (1987)
Muller, R.U., Kubie, J.L., Ranck, J.B.: Spatial firing pattern of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935–1950 (1987)
O’Keefe, J.: Hippocampus function: does the working memory hypothesis work? Should we retire the cognitive map theory? Behav. Brain Sci. 2, 339–343 (1979)
O’Keefe, J., Dostrovsky, J.: The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely moving rat. Brain Res. 34, 171–175 (1971)
O’Keefe, J., Nadel, L.: The hippocampus as a cognitive map. Oxford University Press, London (1978)
Parron, C., Poucet, B., Save, E.: Entorhinal cortex lesions impairs the use of distal but not proximal landmarks during navigation in the rat. Behav. Brain Res. 154, 345–352 (2004)
Paz-Villagrà n, V., Save, E., Poucet, B.: Coding of separate and connected spatial contexts by place cells. Eur. J. Neurosci. 20, 1379–1390 (2004)
Poucet, B.: Searching for spatial unit firing in the prelimbic area of the rat medial prefrontal cortex. Behav. Brain Res. 84, 151–159 (1997)
Poucet, B., Chapuis, N., Durup, M., Thinus-Blanc, C.: A study of exploratory behavior as an index of spatial knowledge in hamsters. Anim. Learn. Behav. 14, 93–100 (1986)
Poucet, B., Lenck-Santini, P.-P., Hok, V., Save, E., Banquet, J.-P., Gaussier, P., Muller, R.U.: Spatial navigation and hippocampal place cell firing: the problem of goal encoding. Rev. Neurosci. 15, 87–109 (2004)
Poucet, B., Lenck-Santini, P.-P., Save, E.: Drawing parallels between the behavioural and neural properties of navigation. In: Jeffery, K.J. (ed.) The neurobiology of spatial behaviour, pp. 187–198. Oxford University Press, Oxford (2003)
Quirk, G.J., Muller, R.U., Kubie, J.L.: The firing of hippocampal place cells in the dark depends on the rat’s recent experience. J. Neurosci. 10, 2008–2017 (1990)
Renaudineau, S., Poucet, B., Save, E.: Effects of a conflict between proximal objects and distal cues on place cell activity (unpublished data)
Rossier, J., Schenk, F., Kaminsky, Y., Bureš, J.: The place preference task: a new tool for studying the relation between behavior and place cell activity in rats. Behav. Neurosci. 114, 273–284 (2000)
Rotenberg, A., Muller, R.U.: Variable coupling to a continuous viewed stimulus: evidence that the hippocampus acts as a perceptual system. Phil. Trans. R Soc. Lond. B 352, 1505–1513 (1997)
Save, E., Cressant, A., Thinus-Blanc, C., Poucet, B.: Spatial firing of hippocampal place cells in blind rats. J. Neurosci. 18, 1818–1826 (1998)
Save, E., Nerad, L., Poucet, B.: Contribution of multiple sensory information to place field stability in hippocampal place cells. Hippocampus 10, 64–76 (2000)
Save, E., Paz-Villagrà n, V., Alexinsky, T., Poucet, B.: Functional interaction between the parietal cortex and hippocampal place cell firing in the rat. Eur. J. Neurosci. 21, 522–530 (2005)
Save, E., Poucet, B.: Hippocampal-parietal cortical interactions in spatial cognition. Hippocampus 10, 491–499 (2000a)
Save, E., Poucet, B.: Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation. Behav. Brain Res. 109, 195–206 (2000b)
Save, E., Poucet, B., Foreman, N., Buhot, M.C.: Object exploration and reactions to spatial and non-spatial changes in hooded rats following damage to parietal cortex or hippocampal formation. Behav. Neurosci. 106, 447–456 (1992)
Shapiro, M.L., Tanila, H., Eichenbaum, H.: Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7, 624–642 (1997)
Sharp, P.E., Blair, H.T., Etkin, D., Tzanetos, D.B.: influences of vestibular and visual motion information on the spatial firing pattern of hippocampal place cells. J. Neurosci. 15, 173–189 (1995)
Sutherland, R.J., Dyck, R.H.: Place navigation by rats. Can J. psychol. 38, 322–347 (1984)
Suzuki, S., Augerinos, G., Black, A.H.: Stimulus control of spatial behavior in the eight-arm maze in rats. Learn Motiv. 11, 1–18 (1980)
Tanila, H., Shapiro, M.L., Eichenbaum, H.: Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7, 613–623 (1997)
Thinus-Blanc, C., Bouzouba, L., Chaix, K., Chapuis, N., Durup, M., Poucet, B.: A study of spatial parameters encoded during exploration in hamsters. J. Exp. Psychol: Anim. Behav. Proc. 13, 418–427 (1987)
Tolman, E.C.: Cognitive maps in rats and men. Psychol. Rev. 55, 189–208 (1948)
Touretzky, D.S., Redish, A.D.: Theory of rodent navigation based on interacting representations of space. Hippocampus 6, 247–270 (1996)
Trullier, O., Wiener, S.I., Berthoz, A., Meyer, J.-A.: Biologically artificial navigation systems: review and prospects. Prog. Neurobiol. 51, 483–544 (1997)
Whishaw, I.Q.: Spatial mapping takes time. Hippocampus 8, 122–130 (1998)
Wiener, S.I., Korshunov, V.A., Garcia, R., Berthoz, A.: Inertial substratal and landmark cue control of hippocampal CA1 place cell activity. Eur. J. Neurosci. 7, 2206–2219 (1995)
Zinyuk, L., Kubik, S., Kaminsky, Y., Fenton, A.A., Bureš, J.: Understanding hippocampal activity by using purposeful behavior: place navigation induce vs. place cell discharge in both task-relevant and task-irrelevant spatial reference frames. Proc. Natl. Acad. Sci. 97, 3771–3776 (2000)
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Save, E., Hok, V., Renaudineau, S., Parron, C., Poucet, B. (2007). Cue and Goal Encoding in Rodents: A Source of Inspiration for Robotics?. In: Jefferies, M.E., Yeap, WK. (eds) Robotics and Cognitive Approaches to Spatial Mapping. Springer Tracts in Advanced Robotics, vol 38. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-75388-9_10
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DOI: https://doi.org/10.1007/978-3-540-75388-9_10
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