Abstract
We have each recently proposed models of hippocampal function. The central concept of Gray’s model is that the septohippocampal system, together with the Papez circuit, functions as a comparator detecting departures from expectation in respect to both stimulus—stimulus and response—stimulus relationships. Rawlins’s model, in contrast, treats the hippocampal formation as a high-capacity, intermediate-term memory buffer. The principal aim of this chapter is to consider ways in which the two models may perhaps be integrated. We shall first present brief summaries of the two models (fuller accounts, including reviews of the data on which the models are based, are available elsewhere: Gray, 1982a,b; Rawlins, 1985). Gray’s model is given a relatively more detailed treatment as it is the more far-ranging.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Albert, D. J., Brayley, K. N., and Milner, J. A. Connections from the lateral septum modulating reactivity in the rat. Physiology and Behavior, 1978, 21, 761–767.
Alger, B. E., and Teyler, T. J. Long-term and short-term plasticity in the CA1, CA3 and dentate regions of the rat hippocampal slice. Brain Research, 1976, 110, 463–480.
Altman, J., Brunner, R. L., and Bayer, S. A. The hippocampus and behavioral maturation. Behvioral Biology, 1973, 8, 557–596.
Amsel, A. Frustrative nonreward in partial reinforcement and discrimination learning: Some recent history and a theoretical extension. Psychological Review, 1962, 69, 306–328.
Andersen, P. Long-lasting facilitation of synaptic transmission. In K. Elliot and J. Whelan (Eds.), Functions of the septo-hippocampal system. Ciba Foundation Symposium 58 (n.s.). Amsterdam: Elsevier, 1978, pp. 87–82.
Assaf, S. Y., and Miller, J. J. Neuronal transmission in the dentate gyrus: Role of inhibitory mechanisms. Brain Research, 1978, 151, 587–592.
Assaf, S. Y., Mason, S. T., and Miller, J. J. Noradrenergic modulation of neuronal transmission between the entorhinal cortex and the dentate gyrus of the rat. Journal of Physiology, 1979, 292, P52.
Berger, T. W., and Thompson, R. F. Neuronal plasticity in the limbic system during classical conditioning of the rabbit nictitating membrane response. I. The hippocampus. Brain Research, 1978a, 145, 323–346.
Berger, T. W., and Thompson, R. F. Neuronal plasticity in the limbic system during classical conditioning of the rabbit nictitating membrane response. II. Septum and mammilary bodies. Brain Research, 1978b, 156, 293–314.
Boitano, J. J., Dolka, C. J. P., Mulinski, P., Misikomis, S., and Kaluzynski, T. E. Effects of hippocampectomy in an incremental-step DRL paradigm. Physiology and Behavior, 1980, 25, 273–278.
Bowery, N. G. (Ed.). Actions and interactions of GABA and benzodiazepines. New York: Raven Press, 1984.
Braestrup, C., and Squires, R. F. Specific benzodiazepine receptors in rat brain characterized by high-affinity [3H]-diazepam binding. Proceedings of the National Academy of Sciences USA, 1977, 74, 3805–3809.
Brayley, K. N., and Albert, D. J. Suppression of VMH-lesion-induced reactivity and aggressiveness in the rat by stimulation of lateral septum, but not medial septum or cignulate cortex. Journal of Comparative and Physiological Psychology, 1977, 91, 290–299
Brown, J., Lewis, V., Brown, M., Horn, G., and Bowes, J. P. A comparison between transient amnesias induced by two drugs (diazepam and lorazepam) and amnesia of organic orgin. Neuropsychologia, 1982, 20, 55–70.
Butters, N., and Cermack, L. S. Some analyses of amnesic syndromes in brain-damaged patients. In R. L. Isaacson and K. H. Pribram (Eds.), The hippocampus, Vol. 2: Neurophysiology and behavior. New York: Plenum Press, 1975, pp. 377–409.
Capaldi, E. J. A sequential hypothesis of instrumental learning. In K. W. Spence and J. T. Spence (Eds.), The psychology of learning and motivation, Vol. 1. New York: Academic Press, 1967, pp. 67–156.
Cooper, S. J. Benzodiazepines as appetite-enhancing compounds. Appetite, 1980, 1, 7–19.
Costa, E., and Greengard, P. (Eds.). Mechanism of action of benzodiazepines. New York: Raven Press, 1975.
Dabrowska, J., and Drzewiecka, B. Comparison of the septal lesion effects on visual and spatial discrimination in rats. Acta Neurobiologiae Experimentalis, 1975, 35, 255–274.
Davis, N. M., Brooks, S., Gray, J. A., and Rawlins, J. N. P. Chloridiazepoxide and resistance to punishment. Quarterly Journal of Experimental Psychology, 1981, 33B, 227–239.
Dickinson, A. Response supression and facilitation by aversive and stimuli following septal lesions in rats: A review and model. Physiological Psychology, 1974, 2, 444–456.
Douglas, R. J. The hippocampus and behavior. Psychological Bulletin, 1967, 67, 416–442.
Elliot, K., and Whelan, J. (Eds.). Functions of the septo-hippocampal system. Ciba Foundation Symposium, 58 (n.s.). Amsterdam: Elsevier, 1978.
Feldon, J., and Gray, J. A. Effects of medial and lateral and septal lesions on the partial reinforcement extinction effect at short inter-trial intervals. Quarterly Journal of Experimental Psychology, 1979a, 31, 675–690.
Feldon, J., and Gray, J. A. Effects of medial and lateral septal lesions on the partial reinforcement extinction effect at one trial a day. Quarterly Journal of Experimental Psychology, 1979b, 31, 653–674.
Feldon, J., and Gray, J. A. The partial reinforcement extinction effect after treatment with chlordiazepoxide. Psychopharmacology, 1981, 73, 269–275.
Gabriel, M., Miller, J.D., and Saltwick, S. E. Unit activity in cingulate cortex and anteroventral thalamus of the rabbit during differential conditioning and reversal. Journal of Comparative and Physiological Psychology, 1977, 91, 423–433.
Gabriel, M., Foster, K., Orona, E., Saltwick, S. E., and Stanton, M. Neuronal activity of cingulate cortex, anteroventral thalamus, hippocampal formation and discriminative conditioning: Encoding and the extraction of the significance of conditional stimuli. In J. M. Sprague and A. Epstein (Eds.), Progress in psychobiology and physiological psychology, Vol. 9. New York: Academic Press, 1980, pp. 125–231.
Gaffan, D. Loss of recognition memory in rats with lesions of the fornix. Neuropsychologia, 1972, 10, 327–341.
Gaffan, D. Monkey’s recognition memory for complex pictures and the effect of fornix transection. Quarterly Journal of Experimental Psychology, 1977a, 29, 505–514.
Gaffan, D. Recognition memory after short retention intervals in fornix-transected monkeys. Quarterly Journal of Experimental Psychology, 1979b, 29, 577–588.
Gaffan, D. Hippocampus: Memory habit and voluntary movement. In L. Weiskrantz (Ed.), Animal intelligence. Phil. Trans. Royal Soc. B, 1985, 308, 87–99.
Graeff, F. G., Quintero, S., and Gray, J. A. Median raphe stimulation, hippocampal theta rhythm and threat-induced behavioral inhibition. Physiology and Behavior, 1980, 25, 253–261.
Grastyan, E., Lissak, K., Madarasz, I. and Donhoffer, H. Hippocampal electrical activity during the development of conditioned reflexes. Electroencephalography and Clinical Neuro-physiology, 1959, 11, 409–430.
Gray, J. A. Sodium amobarbital, the hippocampal theta rhythm and the partial reinforcement extinction effect. Psychological Review, 1970, 77, 465–480.
Gray, J. A. Effects of septal driving of the hippocampal theta rhythm on resistance to extinction. Physiology and Behavior, 1972, 8, 481–490.
Gray, J. A. Elements of a two-process theory of learning. London: Academic Press, 1975.
Gray, J. A. Drug effects on fear and frustration: Possible limbic site of action of minor tranquillizers. In L. L. Iversen, S. D. Iversen, and S. H. Snyder (Eds.), Handbook of psychopharmacology, Vol. 8: Drugs, neurotransmitters, and behavior. New York: Plenum Press, 1977, pp. 433–529.
Gray, J. A. Anxiety and the brain: Not by neurochemistry alone. Psychological Medicine, 1979a, 9, 605–609.
Gray, J. A. Spatial mapping only a special case of hippocampal function. Behavioral and Brain Sciences, 1979b, 2, 501–503.
Gray, J. A. The neuropsychology of anxiety. Oxford: Oxford University Press, 1982a.
Gray, J. A. Precis of the neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system. Behavioral and Brain Sciences, 1982b, 5, 469–484.
Gray, J. A. On mapping anxiety. Behavioral and Brain Sciences, 1982c, 5, 506–525.
Gray, J. A. The hippocampus as an interface between cognition and emotion. In H. L. Roitblat, T. G. Bever, and H. S. Terrace (Eds.), Animal cognition. Hillsdale, NJ: Erlbaum, 1984, pp. 607–626.
Gray, J. A., and McNaughton, N. Comparison between the behavioural effects of septal and hippocampal lesions: A review. Neuroscience and Biobehavioral Reviews, 1983, 7, 119–188.
Gray, J. A., Mcnaughton, N., James, D. T. D., and Kelly, P. H. Effect of minor tranquillisers on hippocampal theta rhythm mimicked by depletion of forebrain noradrenaline. Nature, 1975, 258, 424–425.
Gray, J. A., Feldon, J., Rawlins, J. N. P., Owen, S., and McNaughton, N. The role of the septo-hippocampal system and its noradrenergic afferents in behavioural responses to nonreward. In K. Elliott and J. Whelan (Eds.), Functions of the septo-hippocampal system. Ciba Foundation Symposium 58 (n.s.). Amsterdam: Elsevier, 1978, pp. 275–300.
Gray, J. A., Quintero, S., and Mellanby, J. Gamma-aminobutyrate, the benzodiazepines and the septo-hippocampal system. In M. Trimble (Ed.), Benzodiazepines divided. Chichester: Wiley, 1983, pp. 101–127.
Gray, J. A., Quintero, S., Mellanby, J., Buckland, C., Fillenz, M., and Fung, S. C. Some biochemical, behavioural and electrophysiological tests of the GABA hypothesis of anti-anxiety drug action. In N. G. Bowery (Ed.), Actions and interactions of GABA and benzodiazepines. New York: Raven Press, 1984.
Green, J. S., and Arduini, A. Hippocampal electrical activity in arousal. Journal of Neurophysiology, 1954, 17, 533–557.
Haefely, W., Pieri, L., Polc, P., and Schaffner, R. General pharmacology and neuropharmacology of benzodiazepine derivatives. In F. Hoffmeister and G. Stille (Eds.), Handbook of experimental pharmacology. Berlin: Springer-Verlag, 1981.
Henke, P. G. Persistence of runway performance after septal lesions in rats. Journal of Comparative and Physiological Psychology, 1974, 86, 760–767.
Hill, A. J. First occurrence of hippocampal spatial firing in a new environment. Experimental Neurology, 1978, 62, 282–297.
Hirsch, R., and Krajden, J. The hippocampus and the expression of knowledge. In R. L. Isaacson and N. E. Spear (Eds.), The expression of knowledge. New York: Plenum Press, 1982, pp. 213–241.
Hirsch, R. The hippocampus and contextual retrieval of information from memory: A theory. Behavioural Biology, 1974, 12, 421–444.
Horel, J. A. The neuroanatomy of amnesia: A critique of the hippocampal memory hypothesis. Brain, 1978, 101, 403–445.
Jaffard, R., Destrade, C., Durkin, T., and Ebel, A. Memory formation as related to genotypic or experimental variations of hippocampal cholinergic activity in mice. Physiology and Behaviour, 1979, 22, 1093–1096.
Jarrard, L. E., and Isaacson, R. L. Hippocampal ablation in rats: Effects of intertrial interval. Nature (London), 1965, 207, 109–110.
Kaada, B. R., Jansen, J., and Anderson, P. Stimulation of the hippocampus and medial cortical areas in unanesthetized cats. Neurology, 1953, 3, 844–857.
Kelly, A. E., and Domesick, V. B. The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: An anterograde-and retrograde-horseradish peroxidase study. Neuroscience, 1982, 7, 2321–2335.
Kimble, D. P. Possible inhibitory functions of the hippocampus. Neuropsychologia, 1969, 7, 235–244.
Kimble, D. P. Choice behavior in rats with hippocampal lesions. In R. L. Isaacson and K. H. Pribram (Eds.), The hippocampus, Vol. 2: Neurophysiology and behavior, New York: Plenum Press, 1975, pp. 309–326.
Köhler, C., Shipley, M. T., Srebro, B., and Harkmark, W. Some retrohippocampal afferents to the entorhinal cortex: Cells of origin studied by the HRP method in the rat and mouse. Neuroscience Letters, 1978, 10, 115–120.
Landfield, P. W. Synchronous EEG rhythms: Their nature and possible functions in memory, information transmission and behavior. In W. H. Gispen (Ed.), Molecular and Functional Neurobiology. Amsterdam: Elsevier, 1976, pp. 387–424.
McCleary, R. A. Response-modulating functions of the limbic system: Initiation and suppression. In E. Stellar and J. M. Sprague (Eds.), Progress in physiological psychology, Vol. 1. New York: Academic Press, 1966.
McNaughton, N., and Mason, S. T. The neuropsychology and neuropharmacology of the dorsal ascending noradrenergic bundle—A review. Progress in Neurobiology, 1980, 14, 157–219.
McNaughton, N., James, D. T., Stewart, J., Gray, J. A., Valero, I., and Drewnowski, A. Septal driving of hippocampal theta rhythm as a function of frequency in the male rat: Effects of drugs. Neuroscience, 1977, 2, 1019–1027.
Meibach, R. C., and Siegel, A. Subicular projections to the posterior cingulate cortex in rats. Experimental Neurology, 1977, 57, 264–274.
Mellanby, J., Gray, J. A., Quintero, S., Holt, L., and McNaughton, N. Septal driving of the hippocampal theta rhythm: A role for gamma-aminobutyrate in the effects of minor tranquillizers? Neuroscience, 1981, 6, 1413–1421.
Mikulka, P. J., and Freeman, F. G. The effects of reinforcement delay and hippocampal lesions on the acquisition of a choice response. Behavioral Biology, 1975, 15, 473–477.
Milner, B. The memory deficit in bilateral hippocampal lesions. Psychiatric Research Reports, 1959, 11, 43–58.
Milner, B. Preface: Material specific and generalized memory loss. Neuropsychologia, 1968, 6, 175–179.
Milner, B. Memory and the medial temporal regions of the brain. In K. H. Pribram and D. E. Broadbent (Eds.), Biology of memory. New York: Academic Press, 1970, pp. 29–50.
Mishkin, M. Memory in monkeys severely impaired by combined but not separate removal of amygdala and hippocampus. Nature, 1978, 273, 297–298.
Mitchell, S. J., and Ranck, J. B., Jr. Generation of theta rhythm in medial entorhinal cortex of freely-moving rats. Brain Research, 1980, 189, 49–66.
Mitchell, S. J., Rawlins, J. N. P., Steward, O., and Olton, D. S. Medial septal lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats. Journal of Neuroscience, 1982, 2, 292–302.
Mohler, H., and Okada, T. Benzodiazepine receptor: Demonstration in the central nervous system. Science, 1977, 198, 849–851.
Nadel, L., and O’Keefe, J. The hippocampus in pieces and patches: An essay on modes of explanation in physiological psychology. In R. Bellairs and E. G. Gray (Eds.), Essays on the nervous system: A festschrift for Professor J. Z. Young. Oxford: Clarendon Press, 1974.
Newman, J. P., Gorenstein, E. E., and Kelsey, J. E. Failure to delay gratification following septal lesions in rats: Implications for an animal model of disinhibitory psychopathology. Personality and Individual Differences, 1983, 4, 147–156.
Niki, H., and Watanabe, M. Cingulate unit activity and delayed response. Brain Research, 1976, 110, 381–386.
O’Keefe, J., and Dostrovsky, J. The hippocampus as a spatial map: Preliminary evidence from unit activity in the free-moving rat. Brain Research, 1971, 34, 171–175.
O’Keefe, J., and Nadel, L. The hippocampus as a cognitive map. Oxford: Clarendon Press, 1978.
Olton, D. S. Characteristics of spatial memory. In S. H. Hulse, H. Fowler, and W. K. Honig (Eds.), Cognitive processes in animal behavior. Hillsdale, NJ: Erlbaum, 1978a, pp. 341–373.
Olton, D. S. The function of septo-hippocampal connections in spatially organized behaviour. In K. Elliot and J. Whelan (Eds.), Functions of the septo-hippocampal system. Ciba Foundation Symposium 58 (n.s.). Amsterdam: Elsevier, 1978b, pp. 327–342.
Olton, D. S. Functions of the septo-hippocampal system. Behavioural and Brain Sciences, 1982, 3, 494–495.
Olton, D. S., and Samuelson, R. J. Remembrance of places past: Spatial memory in rats. Journal of Experimental Psychology: Animal Behaviour Processes, 1976, 2, 97–116.
Olton, D. S., Becker, J. T., and Handelmann, G. E. Hippocampus, space, and memory. Behavioural and Brain Sciences, 1979, 2, 313–322.
Oscar-Berman, M. O., and Samuels, I. Stimulus preference and memory factors in Korsakoffs syndrome. Neuropsychologia, 1977, 15, 99–106.
Owen, M. J., and Butler, S. R. Amnesia after transectin of the fornix in monkeys: Long-term memory impaired, short-term memory intact. Behavioural Brain Research, 1981, 3, 115–123.
Papez, J. W. A proposed mechanism of emotion. Archives of Neurology and Psychiatry, 1937, 38, 725–743.
Parmeggiani, P. L., Azzaroni, A., and Lenzi, P. On the functional significance of the circuit of Papez. Brain Research, 1971, 30, 357–374.
Parmeggiani, P. L., Lenzi, P., and Azzaroni, A. Transfer of the hippocampal output by the anterior thalamic nuclei. Brain Research, 1974, 67, 269–278.
Petsche, H., Stumpf, Ch., and Gogolak, G. the significance of the rabbit’s septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells. Electroencephalography and Clinical Neurophysiology, 1962, 14, 202–211.
Quintero, S., Buckland, C., Gray, J. A., McNaughton, N., and Mellanby, J. The effects of compounds related to γ-aminobutyrate and benzodiazepine receptors on behavioural responses to anxiogenic stimuli in the rat: Choice behaviour in the T-maze. Psychopharmacology, 1985a, 86, 328–333.
Quintero, S., Henney, S., Lawson, P., Mellanby, J., and Gray, J. A. The effects of compounds related to γ-aminobutyrate and benzodiazepine receptors on behavioural responses to anxiogenic stimuli in the rat: Punished barpressing. Psychopharmacology, 1985b, 85, 244–251.
Ransom, B. R., and Barker, J. L. Pentobarbital selectively enhances GABA-mediated post-synaptic inhibition in tissue cultured mouse spinal neurons. Brain Research, 1976, 114, 530–535.
Rawlins, J. N. P. Associations across time: The hippocampus as a temporary memory store. Behavioural and Brain Sciences, 1985, 8, 479–496.
Rawlins, J. N. P., and Olton, D. S. The septo-hippocampal system and cognitive mapping. Behavioural Brain Research, 1982, 5, 331–358.
Rawlins, J. N. P., and Tsaltas, E. The hippocampus, time and working memory. Behavioural Brain Research, 1983, 10, 233–262.
Rawlins, J. N. P., Feldon, J., and Gray, J. A. The effects of hippocampectomy and of fimbria section upon the partial reinforcement extinction effect in rats. Experimental Brain Research, 1980a, 8, 273–283.
Rawlins, J. N. P., Feldon, J., Salmon, P., Gray, J. A., and Garrud, P. The effects of chlordiazepoxide HC1 administration upon punishment and conditioned suppression in the rat. Psychopharmacology, 1980b, 70, 317–322.
Rawlins, J. N. P., Winocur, G., and Gray, J. A. The hippocampus, collateral behavior and timing. Behavioral Neuroscience, 1983, 97, 857–872.
Rawlins, J. N. P., Feldon, J., and Butt, S. The effects of delaying reward on choice preference in rats with hippocampal or selective septal lesions. Behavioural Brain Research, 1985a, 15, 191–203.
Rawlins, J. N. P., Feldon, J., Ursin, H., and Gray, J. A. Resistance to extinction after schedules of partial delay or partial reinforcement in rats with hippocampal lesions. Experimental Brain Research, 1985, 59, 273–281.
Rudell, A. P., Fox, S. E., and Ranck, J. B., Jr. Hippocampal excitability phase-locked to the theta-rhythm in walking cats. Experimental Neurology, 1980, 68, 87–96.
Segal, M. Afferents to the entorhinal cortex of the rat studied by the method of retrograde transport of horseradish peroxidase. Experimental Neurology, 1977a, 57, 750–765.
Segal, M. Changes in interhemispheric hippocampal responses during conditioning in the awake rat. Experimental Brain Research, 1977b, 29, 553–565.
Segal, M. The effects of brainstem priming stimulation on interhemispheric hippocampal responses in the awake rat. Experimental Brain Research, 1977c, 28, 529–541.
Segal, M. Excitability changes in rat hippocampus during conditioning. Experimental Brain Research, 1977d, 55, 67–73.
Segal, M. The noradrenergic innervation of the hippocampus. In J. A. Hobson and M. A. B. Brazier (Eds.), The reticular formation revisited. New York: Raven Press, 1980, pp. 415–425.
Sidman, M., Stoddard, L., and Mohr, J. Some additional quantitative observations of immediate memory in a patient with bilateral hippocampal lesions. Neuropsychologia, 1968, 6, 245–254.
Sikorsky, R. D., Donovick, P. J., Burright, R. G., and Chin, T. Experimential effects on acquisition and reversal of discrimination tasks by albino rats with septal lesions. Physiology and Behaviour, 1977, 18, 231–236.
Squires, R. F. Benzodiazepine receptor multiplicity. Neuropharmacology, 1983, 22, 1443–1450.
Swanson, L. W. The anatomical organization of septo-hippocampal projections. In K. Elliot and J. Whelan (Eds.), Functions of the septo-hippocampal system. Ciba Foundation Symposium, 58 (n.s.). Amsterdam: Elsevier, 1978, pp. 25–43.
Thiebot, M-H., Le Bihan, C., Soubrie, P., and Simon, P. Benzodiazepines reduce the tolerance to reward delay in rats. Psychopharmacology, 1985, 86, 147–152.
Ticku, M. K., and Olsen, R. W. Interaction of barbiturates with dihydropicrotoxinin binding sites related to the GABA receptor-ionophone system. Life Sciences, 1978, 22, 1643–1652.
Vanderwolf, C. W. Limbic-diencephalic mechanisms of voluntary movement. Psychological Review, 1971, 78, 83–113.
Vanderwolf, C. H., Kramis, R., and Robinson T. E. Hippocampal electrical activity during waking behaviour and sleep: Analyses using centrally acting drugs. In K. Elliott and J. Whelan (Eds.), Functions of the septo-hippocampal system. Ciba Foundation Symposium, 58 (n.s.) Amsterdam: Elsevier, 1978, pp. 199–221.
Van Hoesen, G. W., Rosene, D. L., and Mesulam, M. M. Subicular input from temporal cortex in the rhesus monkey. Science, 1979, 205, 608–610.
Victor, M., Adams, R. D., and Collins, G. H. The Wernicke-Korsakoff syndrome. Oxford: Blackwell, 1971.
Vinogradova, O. S. Functional organization of the limbic system in the process of registration of information: Facts and hypotheses. In R. L. Isaacson and K. H. Pribram (Eds.), The hippocampus: Vol. 2. Neurophysiology and behavior. New York: Plenum Press, 1975, pp. 1–70.
Walker, D. W., Messer, L. G., Freund, G., and Means, L. W. Effect of hippocampal lesions and intertrial interval on single-alternation performance in the rat. Journal of Comparative and Physiological Psychology, 1972, 80, 469–477.
Weiskrantz, L. A comparison of hippocampal pathology in man and other animals. In K. Elliott and J. Whelen (Eds.), Functions of the septo-hippocampal system. Ciba Foundation Symposium 58 (n.s.). Amsterdam: Elsevier, 1978, pp. 373–387.
Weiskrantz, L., and Warrington, E. K. The problem of the amnesic syndrome in man and animals. In R. L. Isaacson and K. H. Probram (Eds.), The hippocampus: Vol. 2. Neurophysiology and behavior. New York: Plenum Press, 1975, pp. 411–428.
Winocur, G. The amnesic syndrome: A deficit in cue utilization. In L. Cermak (Ed.), Human memory. Hillsdale, NJ: Erlbaum, 1982
Winocur, G., and Breckenridge, C. B. Cue-dependent behaviour of hippocampally damaged rats in a complex maze. Journal of Comparative and Physiological Psychology, 1973, 82, 512–522.
Winocur, G., and Mills, J. A. Transfer between related and unrelated problems following hippocampal lesions in rats. Journal of Comparative and Physiological Psychology, 1970, 73, 162–169.
Winocur, G., and Olds, J. Effects of context manipulation on memory and reversal learning in rats with hippocampal lesions. Journal of Comparative and Physiological Psychology, 1978, 92, 312–321.
Winson, J. Hippocampal theta rhythm. I. Depth profiles in the curarized rat. Brain Research, 1976, 103, 57–70.
Zola-Morgan, S., Squire, L. R., and Mishkin, M. The neuroanatomy of amnesia: Amygdalahippocampus vs. temporal stem. Science, 1982, 218, 1337–1339.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1986 Plenum Press, New York
About this chapter
Cite this chapter
Gray, J.A., Rawlins, J.N.P. (1986). Comparator and Buffer Memory. In: Isaacson, R.L., Pribram, K.H. (eds) The Hippocampus. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-8024-9_6
Download citation
DOI: https://doi.org/10.1007/978-1-4615-8024-9_6
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4615-8026-3
Online ISBN: 978-1-4615-8024-9
eBook Packages: Springer Book Archive