Abstract
In order to compare the relative involvement of prefrontal and temporal regions in spatial memory, rats with bilateral electrolytic lesions of perirhinal cortex, prefrontal cortex, or both regions were tested in the water and radial-arm maze. Perirhinal and prefrontal lesions produced similar performance deficits during water-maze acquisition and in the radial-maze procedure. Perirhinal cortex lesions also disrupted performance in a water-maze probe trial conducted 5 min after four training trials, whereas prefrontal lesions did not. Surprisingly, the combined-lesion group was not impaired during water-maze acquisition and performed significantly better than the perirhinal-lesioned group in the probe trial. This finding is interpreted in terms of the executive function of prefrontal cortex and its possible role in switching behavior between different search strategies, only some of which may be dependent on perirhinal cortex.
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References
Baddeley, A. (1986). Working memory. Oxford: Oxford University Press, Clarendon Press.
Baddeley, A. (1996). The fractionation of working memory. Proceedings of the National Academy of Sciences, 93, 13468–13472.
Baddeley, A., & Della Sala, S. (1996). Working memory and executive control. Philosophical Transactions of the Roval Society of London: Series B, 351, 1397–1403.
Bechara, A., Damasio, H., Tranel, D., & Anderson, S. W. (1998). Dissociation of working memory from decision making within the human prefrontal cortex. Journal of Neuroscience, 18, 428–437.
Benhamou, S. (1994). Spatial memory and searching efficiency. Animal Behaviour, 47, 1423–1433.
Benhamou, S. (1997). Path integration by swimming rats. Animal Behaviour, 54, 321–327.
Buckley, M. J., Gaffan, D., & Murray, E. A. (1997). Functional double dissociation between two inferior temporal areas: Perirhinal cortex versus middle temporal gyrus. Journal of Neurophysiology, 77, 587–598.
Buffalo, E. A., Reber, P. J., & Squire, L. R. (1998). The human perirhinal cortex and recognition memory. Hippocampus, 8, 330–339.
Burwell, R.D., Witter, M. P., & Amaral, D. G. (1995). Perirhinal and postrhinal cortices of the rat: A review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus, 5, 390–408.
Bussey, T. J., Muir, J. L., & Aggleton, J. P. (1999). Functionally dissociating aspects of event memory: The effects of combined perirhinal and postrhinal cortex lesions on object and place memory in the rat. Journal of Neuroscience, 19, 495–502.
de Bruin, J. P. C., Sanchez-Santed, F., Heinsbroek, R. P. W., Donker, A., & Postmes, P. (1994). A behavioural analysis of rats with damage to the medial prefrontal cortex using the Morris water maze: Evidence for behavioural flexibility, but not for impaired spatial navigation. Brain Research, 652, 323–333.
Dudchenko, P. A., Goodridge, J. P., Seiterle, D. A., & Taube, J. S. (1997). Effects of repeated disorientation on the acquisition of spatial tasks in rats: Dissociation between the appetitive radial-arm maze and aversive water maze. Journal of Experimental Psychology: Animal Behavior Processes, 23, 194–210.
Eichenbaum, H., Stewart, C., & Morris, R. G. M. (1990). Hippocampal representation in spatial learning. Journal of Neuroscience, 10, 331–339.
Ennaceur, A., Neave, N., & Aggleton, J. P. (1996). Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behavioural Brain Research, 80, 9–25.
Funahashi, S., Inoue, M., & Kubota, K. (1997). Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation. Behavioural Brain Research, 84, 203–223.
Fuster, J. M., Bauer, R. H., & Jervey, J. P. (1985). Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Research, 330, 299–307.
Gaffan, D. (1998). Ideothetic input into object-place configuration as the contribution to memory of the monkey and human hippocampus: A review. Experimental Brain Research, 123, 201–209.
Glenn, M. J., & Mumby, D. G. (1998). Place memory is intact in rats with perirhinal cortex lesions. Behavioral Neuroscience, 112, 1353–1365.
Goldman, P. S., & Rosvold, H. E. (1970). Localisation of function within the dorsolateral prefrontal cortex of the rhesus monkey. Experimental Neurology, 27, 291–304.
Goldman-Rakic, P. S. (1995). Cellular basis of working memory. Neuron, 14, 477–485.
Granon, S., Vidal, C., Thinus-Blanc, C., Changeux, J., & Poucet, B. (1994). Working memory, response selection, and effortful processing in rats with medial prefrontal lesions. Behavioral Neuroscience, 108, 883–891.
Gutnikov, S. A., Ma, Y. Y., & Gaffan, D. (1997). Temporo—frontal disconnection impairs visual—visual paired association learning but not configurai learning in Macaca monkeys. European Journal of Neuroscience, 9, 1524–1529.
Kahneman, D., Treisman, A., & Gibbs, B. J. (1992). The reviewing of object files: Object-specific integration of information. Cognitive Psychology, 24, 174–219.
Kesner, R. P. (1989). Retrospective and prospective coding of information: Role of the medial prefrontal cortex. Experimental Brain Research, 74, 163–167.
Kesner, R. P., Hunt, M. E., Williams, J. M., & Long, J. M. (1996). Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cerebral Cortex, 6, 311–318.
Kolb, B. (1990). Prefrontal cortex. In B. Kolb & R. C. Tees (Eds.), The cerebral cortex of the rat (pp. 437–458). London: MIT Press.
Leslie, A. M., Xu, F., Tremoulet, P. D., & Scholl, B. J. (1998). Indexing and the object concept: Developing “what” and “where” systems. Trends in Cognitive Sciences, 2, 10–18.
Liu, P., & Bilkey, D. K. (1998a). Excitotoxic lesions centered on perirhinal cortex produce delay-dependent deficits in a test of spatial memory. Behavioral Neuroscience, 112, 512–524.
Liu, P., & Bilkey, D. K. (1998b). Lesions of perirhinal cortex produce spatial memory deficits in the radial maze. Hippocampus, 8, 114–121.
Liu, P., & Bilkey, D. K. (1998c). Perirhinal cortex contributions to performance in the Morris water maze. Behavioral Neuroscience, 112, 304–315.
Liu, P., & Bilkey, D. K. (1999a). The effect of excitotoxic lesions centered on perirhinal cortex in two versions of the radial-arm maze. Behavioral Neuroscience, 113, 672–682.
Liu, P., & Bilkey, D. K. (1999b). Perirhinal cortex lesions produce a delay-dependent deficit in the working memory version of the water maze. Society for Neuroscience Abstracts, 25, 92.
Maguire, E. A., Burgess, N., Donnet, J. G., Franckowiak, R. S. J., Frith, C. D., & O’Keefe, J. (1998). Knowing where and getting there: A human navigation network. Science, 280, 921–924.
Martin, G. M., Harley, C. W., Smith, A. R., Hoyles, E. S., & Hynes, C. A. (1997). Spatial disorientation blocks reliable goal location on a plus maze but does not prevent goal location in the Morris maze. Journal of Experimental Psychology: Animal Behavior Processes, 23, 183–193.
McNaughton, B. L., Chen, L. L., & Markus, E. J. (1991). “Dead reckoning,” landmark learning, and the sense of direction: A neurophysiological and computational hypothesis. Journal of Cognitive Neuroscience, 3, 190–202.
Meunier, M., Bachevalier, J., Mishkin, M., & Murray, E. A. (1993). Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys. Journal of Neuroscience, 13, 5418–5432.
Miller, E. K., Erickson, C. A., & Desimone, R. (1996). Neural mechanisms of visual working memory in prefrontal cortex of the macaque. Journal of Neuroscience, 16, 5154–5167.
Mumby, D. G., & Pinel, J. P. J. (1994). Rhinal cortex lesions and object recognition in rats. Behavioral Neuroscience, 108, 11–18.
Murray, E. A. (1996). What have ablation studies told us about the neural substrates of stimulus memory? Seminars in the Neurosciences, 8, 13–22.
Olton, D. S., & Samuelson, R. J. (1976). Remembrance of places passed: Spatial memory in rats. Journal of Experimental Psychology: Animal Behavior Processes, 2, 97–115.
Olton, D. S., Walker, J. A., & Gage, F. H. (1978). Hippocampal connections and spatial discrimination. Brain Research, 139, 295–308.
Owen, A. M., Morris, R. G., Sahakian, B. J., Polkey, C. E., & Robbins, T. W. (1996). Double dissociations of memory and executive functions in working-memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Brain, 119, 1597–1615.
Parker, A., & Gaffan, D. (1998). Interaction of frontal and perirhinal cortices in visual object recognition memory in monkeys. European Journal of Neuroscience, 10, 3044–3057.
Paxinos, G., & Watson, C. (1986). The rat brain in stereotaxic coordinates (2nd ed.). San Diego: Academic Press.
Ploner, C. J., Gaymard, B. M., Ehrlé, N., Rivaud-Pechoux, S., Baulac, M., Brandt, S. A., Clemenceau, S., Samson, S., & Pierrot-Deseilligny, C. (1999). Spatial memory deficits in patients with lesions affecting the medial temporal neocortex. Annals of Neurology, 45, 312–319.
Prados, J., & Trobalon, J. B. (1998). Locating an invisible goal in a water maze requires at least two landmarks. Psychobiology, 26, 42–48.
Ridley, R. M. (1994). The psychology of perseverative and stereotyped behaviour. Progress in Neurobiology, 44, 221–231.
Sanchez-Santed, F., Bruin, J. P. C., Heinsbroek, R. P. W, & Verwer, R. W. H. (1997). Spatial delayed alternation of rats in a T-maze: Effects of neurotoxic lesions of the medial prefrontal cortex and of T-maze rotations. Behavioural Brain Research, 84, 73–79.
Save, E. (1997). The contribution of visual and inertial mechanisms to navigation in total darkness. Animal Learning & Behavior, 25, 324–334.
Schenk, F., & Morris, R. G. M. (1985). Dissociation between components of spatial memory after recovery from the effects of retrohippocampal lesions. Experimental Brain Research, 58, 11–18.
Seamans, J. K., Floresco, S. B., & Phillips, A. G. (1998). D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. Journal of Neuroscience, 18, 1613–1621.
Shaw, C., & Aggleton, J. P. (1993). The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats. Behavioural Brain Research, 54, 91–102.
Shimamura, A. P. (1995). Memory and the prefrontal cortex. In J. Grafman, K. J. Holyoak, & F. Boller (Eds.), Structure and functions of the human prefrontal cortex (Annals of the New York Academy of Sciences, Vol. 769, pp. 151–159). New York: New York Academy of Sciences.
Whishaw, I. Q., Cassel, J., & Jarrard, L. E. (1995). Rats with fimbria-fornix lesions display a place response in a swimming pool: A dissociation between getting there and knowing where. Journal of Neuroscience, 15, 5779–5788.
Whishaw, I. Q., McKenna, J. E., & Maaswinkel, H. (1997). Hippocampal lesions and path integration. Current Opinion in Neurobiology, 7, 228–234.
Wiig, K. A., & Bilkey, D. K. (1994a). Effects of perirhinal cortex lesions on spatial reference memory in the rat. Behavioural Brain Research, 63, 101–109.
Wiig, K. A., & Bilkey, D. K. (1994b). Perirhinal cortex lesions in rats disrupt performance in a spatial DNMS task. NeuroReport, 5, 1405–1408.
Wiig, K. A., & Bilkey, D. K. (1995). Lesions of the rat perirhinal cortex exacerbate the memory deficit observed following damage to the fimbria-fornix. Behavioral Neuroscience, 109, 620–630.
Wise, S. P., & Murray, E. A. (1999). Role of the hippocampal system in conditional motor learning: Mapping antecedents to action. Hippocampus, 9, 101–117.
Zar, J. H. (1996). Biostatistical analysis (3rd ed.). New Jersey: Prentice-Hall.
Zola-Morgan, S., Squire, L. R., Amaral, D. G., & Suzuki, W. A. (1989). Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. Journal of Neuroscience, 9, 4355–4370.
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This research was supported by a grant from the New Zealand Lottery Grants Board and the Health Research Council to D.K.B. We thank Barry Dingwall, Chris Perk, Lindsay Robertson, Brendon Sturgeon, Matthew Johnston, Rachel Kyd, and Sara-Lee Illingworth for their help.
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Bilkey, D.K., Liu, P. The effects of separate and combined perirhinal and prefrontal cortex lesions on spatial memory tasks in the rat. Psychobiology 28, 12–20 (2000). https://doi.org/10.3758/BF03330625
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DOI: https://doi.org/10.3758/BF03330625