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The effects of stimulus novelty and familiarity on neuronal activity in the amygdala of monkeys performing recognition memory tasks

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Abstract

The function of the amygdala in behavioural responses to novel stimuli and its possible function in recognition memory were investigated by recording the responses of 659 amygdaloid neurons in monkeys performing recognition memory and visual discrimination tasks. The aim was to determine the contribution of the amygdala in the encoding of familiarity and therefore its role in supporting memory-related neuronal mechanisms in the basal forebrain. The responses of three groups of neurons reflected different forms of memory. One group (n= 10) responded maximally to novel stimuli and significantly less so to the same stimuli when they were familiar. The calculated memory spans of these neurons were in the range of 2–10 intervening trials, and this shortterm retention of information may reflect the operation of a neural mechanism encoding memory for the recency of stimulus presentation. Two other groups responded to the sight of particular categories of familiar stimuli: to foods (n = 6) or to faces (n = 10). The responses of some of these stimulus-selective neurons declined with repeated presentations of foods (3/4 tests) and faces (2/6 tests). The activity of these latter two groups of neurons may be involved in behavioural responses to familiar visual stimuli, particularly when such stimuli have affective or motivational significance. We conclude that the neurophysiological data provide evidence of amygdaloid mechanisms for the recognition of recently seen visual stimuli. However, these amygdaloid mechanisms do not appear to be sufficient to support the performance of long-term recognition memory tasks without additional and complementary functions carried out by other ventromedial temporal, prefrontal and diencephalic structures which also project to the basal forebrain.

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References

  • Aggleton JP, Mishkin M (1983) Memory impairments following restricted medial thalamic lesions in monkeys. Exp Brain Res 52:199–209

    Google Scholar 

  • Aggleton JP, Mishkin M (1986) The Amygdala: sensory gateway to the emotions. In: Plutchik R (ed) Biological foundations of emotion. Academic, New York London, pp 281–299

    Google Scholar 

  • Aggleton JP, Passingham RE (1981) Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta). J Comp Physiol Psychol 95:961–977

    Google Scholar 

  • Aggleton JP, Burton MJ, Passingham RE (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 190:347–368

    Google Scholar 

  • Aggleton JP, Desimone R, Mishkin M (1986) The origin, course and termination of the hippocampothalamic projections in the macaque. J Comp Neurol 242:409–421

    Google Scholar 

  • Aigner TG, Mitchell SJ, Aggleton JP, DeLong MR, Struble RG, Price DL, Wenk GL, Pettigrew, Mishkin M (1991) Transient impairment of recognition memory following ibotenic-acid lesions of the basal forebrain in macaques. Exp Brain Res 86:18–26

    Google Scholar 

  • Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders; the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1–39

    Google Scholar 

  • Bachevalier J, Mishkin M (1986) Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys. Behav Brain Res 20:249–261

    Google Scholar 

  • Bachevalier J, Parkinson JK, Mishkin M (1985) Visual recognition in monkeys: effects of separate vs. combined transection of fornix and amygdalofugal pathways. Exp Brain Res 57:554–561

    Google Scholar 

  • Baylis GC, Rolls ET (1987) Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks. Exp Brain Res 65:614–622

    Google Scholar 

  • Ben-Ari Y, Le Gal La Salle G (1974) Lateral amygdala unit activity. 11. Habituating and non-habituating neurons. Electroencephalogr Clin Neurophysiol 37:449–461

    Google Scholar 

  • Brown MW, Wilson FAW, Riches IP (1987) Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory. Brain Res 409:158–162

    Google Scholar 

  • Bruning JL, Kintz BL (1977) Computational handbook of statistics, 2nd edn. Scott/Foresman, Glenview, Illinois

    Google Scholar 

  • Clugnet M-C, LeDoux JE (1990) Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body. J Neurosci 10:2818–2824

    Google Scholar 

  • Corkin S (1984) Lasting consequences of bilateral temporal lobectomy: clinical course and experimental findings in H.M. Semin Neurol 4:249–259

    Google Scholar 

  • Creutzfeldt O, Bell F, Adey WR (1963) The activity of neurons in the amygdala of the cat following afferent stimulation. In: Bargmann W, Schade JP (eds) The rhinencephalon and related structures. Prog Brain Res 3:31–49

  • Desimone R, Albright TD, Gross CG, Bruce CJ (1984) Stimulus-selective responses of inferior temporal neurons in the macaque. J Neurosci 4:2051–2062

    Google Scholar 

  • Duyckaerts C, Derouesne C, Signoret JL, Gray F, Escoureolle R, Castaigne P (1985) Bilateral and limited amygdalohippocampal lesions causing a pure amnesic syndrome. Ann Neurol 18:314–319

    Google Scholar 

  • Freed DM, Corkin S, Cohen NJ (1987) Forgetting in H.M.: a second look. Neuropsychologia 25:461–471

    Google Scholar 

  • Gaffan D (1985) Hippocampus: memory, habit and voluntary movement. Philos Trans R Soc Lond [Biol.] 308:87–99

    Google Scholar 

  • Gaffan D, Gaffan EA, Harrison S (1989) Visual-visual associative learning and reward-association learning in monkeys: the role for the amygdala. J Neurosci 9:558–564

    CAS  PubMed  Google Scholar 

  • Gloor P, Olivier A, Quesney LF, Andermann F, Horowitz S (1982) The role of the limbic system in experiential phenomena of temporal lobe epilepsy. Ann Neurol 12:129–144

    Google Scholar 

  • Gower EC (1989) Efferent projections from limbic cortex of the temporal pole to the magnocellular medial dorsal nucleus in the rhesus monkey. J Comp Neurol 280:343–358

    Google Scholar 

  • Halgren E, Walter RD, Cherlow DG, Crandall PH (1978) Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain 101:83–117

    Google Scholar 

  • Herzog AG, Van Hoesen GW (1976) Temporal neocortical afferent connections to the amygdala in the rhesus monkey. Brain Res 115:57–69

    Google Scholar 

  • Hitchcock E, Cairns V (1973) Amygdalotomy. Postgrad Med J 49:894–904

    Google Scholar 

  • Horel JA, Keating EG, Misantone LJ (1975) Partial Kluver-Bucy syndrome produced by destroying temporal cortex or amygdala. Brain Res 94:347–359

    Google Scholar 

  • Horel JA, Pytko-Joiner DE, Voytko M, Salsbury K (1987) The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behav Brain Res 23:29–42

    Google Scholar 

  • Me E, Markowitsch HJ (1987) Basal forebrain-lesioned monkeys are severely impaired in tasks of association and recognition memory. Ann Neurol 22:735–743

    Google Scholar 

  • Iwai E, Yukie M (1987) Amygdalofugal and amygdalopetal connections with modality-specific visual cortical area in macaques (Macaca fuscata, M. mulatta, and M. fascicularis). J Comp Neurol 261:362–387

    Google Scholar 

  • Jacobs BL, McGinty DJ (1972) Participation of the amygdala in complex stimulus recognition and behavioural inhibition: evidence from single unit studies. Brain Res 36:431–436

    Google Scholar 

  • Jacobson R (1986) Disorders of facial recognition, social behaviour and affect after combined bilateral amygdalotomy and subcaudate tractotomy — a clinical and experimental study. Psych Med 16:439–450

    Google Scholar 

  • Jones B, Mishkin M (1972) Limbic lesions and the problem of stimulus-reinforcement associations. Exp Neurol 36:362–377

    Article  CAS  PubMed  Google Scholar 

  • Jones EG, Powell TPS (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93:793–820

    CAS  PubMed  Google Scholar 

  • Kling A (1972) Effects of amygdalectomy on social-affective behavior in non-human primates. In: Eleftheriou B (ed) The neurobiology of the amygdala. Plenum, New York, pp 611–632

    Google Scholar 

  • Leonard CM, Rolls ET, Wilson FAW, Baylis GC (1985) Neurons in the amygdala of monkeys with responses selective for faces. Behav Brain Res 15:159–176

    Google Scholar 

  • Mark V, Ervin FR (1970) Violence and the brain. Harper & Row, New York

    Google Scholar 

  • Mesulam M-M, Mufson EJ (1984) Neural inputs into the nucleus basalis of the substantia innominata (CH4) in the rhesus monkey. Brain 107:257–274

    Google Scholar 

  • Miller EK, Li L, Desimone R (1991) A neural mechanism for working and recognition memory in inferior temporal cortex. Science 254:1377–1379

    Google Scholar 

  • Mishkin M (1978) Memory in monkeys severely impaired by combined but not separate removal of amygdala and hippocampus. Nature 273:297–299

    Google Scholar 

  • Mishkin M (1982) A memory system in the monkey. Philos Trans R Soc Lond [Biol] 298:89–95

    Google Scholar 

  • Miyashita Y, Chang HS (1988) Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature 331:68–70

    Google Scholar 

  • Miyashita Y, Rolls ET, Cahusac PMB, Niki H, Feigenbaum JD (1989) Activity of hippocampal formation neurons in the monkey related to a conditional spatial response task. J Neurophysiol 61:669–677

    Google Scholar 

  • Murray EA (1990) Representational memory in nonhuman primates. In: Kesner RP, Olton DS (eds) Neurobiology of comparative cognition. Erlbaum, Hillsdale New Jersey, pp 127–155

    Google Scholar 

  • Murray EA, Mishkin M (1984) Severe tactual as well as visual memory deficits following combined removal of the amygdala and hippocampus in monkeys. J Neurosci 4:2565–2580

    Google Scholar 

  • Murray EA, Mishkin M (1986) Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy. J Neurosci 6:1991–2003

    Google Scholar 

  • Nakamura K, Mikami A, Kubota K (1992) Activity of single neurons in the monkey amygdala during performance of a visual discrimination task. J Neurophysiol 67:1447–1463

    Google Scholar 

  • Nishijo H, Ono T, Nishino H (1988) Topographic distribution of modality-specific amygdalar neurons in the alert monkey. J Neurosci 8:3556–3569

    Google Scholar 

  • O'Keefe J, Bouma H (1969) Complex sensory properties of certain amygdala units in the freely moving cat. Exp Neurol 23:384–398

    Google Scholar 

  • Parkinson JK, Murray EA, Mishkin M (1988) A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci 8:4159–4167

    Google Scholar 

  • Price JL, Amaral DG (1981) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242–1259

    CAS  PubMed  Google Scholar 

  • Riches IP, Wilson FAW, Brown MW (1991) The effects of visual stimulation and memory on neurones of the hippocampal formation and the neighbouring parahippocampal gyrus and inferior temporal cortex of the primate. J Neurosci 11:1763–1779

    Google Scholar 

  • Rolls ET (1990a) A theory of emotion and its application to understanding the neural basis of emotion. Cogn Emotion 4:161–190

    Google Scholar 

  • Rolls ET (1990b) Functions of the primate hippocampus in spatial processing and memory. In: Kesner RP, Olton DS (eds) Neurobiology of comparative cognition. Erlbaum, Hillsdale New Jersey, pp 339–362

    Google Scholar 

  • Rolls ET (1990c) The representation of information in the temporal lobe visual cortical areas of macacques. In: Eckmiller R (ed) Advanced neural computers. North-Holland, Amsterdam New York, pp 69–78

    Google Scholar 

  • Rolls ET, Perrett DI, Caan AW, Wilson FAW (1982) Neuronal responses related to visual recognition. Brain 105:611–646

    Google Scholar 

  • Rolls ET, Miyashita Y, Cahusac PMB, Kesner RP, Niki H, Feigenbaum JD, Bach L (1989) Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown. J Neurosci 9:1835–1845

    CAS  PubMed  Google Scholar 

  • Russchen FT, Amaral DG, Price JL (1985) The afferent connections of the substantia innominata in the monkey, Macaca, fascicularis. J Comp Neurol 242:1–27

    Google Scholar 

  • Sanghera MK, Rolls ET, Roper-Hall A (1979) Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Exp Neurol 63:610–626

    Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–22

    Google Scholar 

  • Spiegler BJ, Mishkin M (1981) Evidence for the sequential participation of inferior temporal cortex and amygdala in the acquisition of stimulus-reward associations. Behav Brain Res 3:303–317

    Article  CAS  PubMed  Google Scholar 

  • Squire LR, Zola-Morgan S (1983) The neurology of memory: the case for correspondence between the findings for human and nonhuman primate. In: Deutsch JA (ed) The physiological basis of memory, 2nd edn. Academic New York London

    Google Scholar 

  • Tranel D, Hyman BT (1990) Neuropsychological correlates of bilateral amygdala damage. Arch Neurol 47:349–355

    Google Scholar 

  • Turner BH, Mishkin M, Knapp M (1980) Organisation of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J Comp Neurol 191:515–543

    Google Scholar 

  • Van Hoesen GW, Pandya DN (1975) Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices in the rhesus monkey. 1. Temporal lobe afferents. Brain Res 95:1–24

    Google Scholar 

  • Weiskrantz L (1956) Behavioral changes associated with the ablation of the amygdaloid complex in monkeys. J Comp Physiol Psychol 49:381–391

    Google Scholar 

  • Wilson FAW, Goldman-Rakic PS (1993) Viewing preferences of rhesus monkeys related to memory for complex pictures, colours and faces (submitted)

  • Wilson FAW, Rolls ET (1987) Habituation and stimulus-specific neuronal responses recorded from the amygdala of the monkey. Soc Neurosci Abstr 17:305.6

    Google Scholar 

  • Wilson FAW, Rolls ET (1990a) Neuronal responses related to the novelty and familiarity of visual stimuli in the substantia innominata, diagonal band of Broca and periventricular region of the primate forebrain. Exp Brain Res 80:104–120

    Google Scholar 

  • Wilson FAW, Rolls ET (1990b) Learning and memory are reflected in the responses of reinforcement-related neurons in the primate basal forebrain. J Neurosci 10:1254–1267

    Google Scholar 

  • Wilson FAW, Rolls ET (1990c) Neuronal responses related to reinforcement in the primate basal forebrain. Brain Res 509:213–223

    Google Scholar 

  • Wilson FAW, Rolls ET (1993) The primate amygdala and reinforcement: a dissociation between rule-based and associatively-mediated memory reflected in neuronal activity (submitted)

  • Wilson FAW, Riches IP, Brown MW (1988) Neuronal activity in the inferomedial temporal cortex compared with that in the hippocampal formation: implications for amnesia of medial temporal lobe origin. In: Woody CD, Alkon DL, McGaugh JL (eds) Cellular mechanisms of conditioning and behavioral plasticity. Plenum, New York, pp 313–328

    Google Scholar 

  • Wilson FAW, Riches IP, Brown MW (1990) Hippocampus and medial temporal cortex: neuronal responses related to behavioural responses during the performance of memory tasks by primates. Behav Brain Res 40:7–28

    Google Scholar 

  • Woodward RR, Goldsmith PL (1964) Cumulative sum techniques. Mathematical and statistical techniques for industry. ICI monographs, No. 3. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Zola-Morgan S, Squire LR (1985) Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. Behav Neurosci 99:22–34

    Google Scholar 

  • Zola-Morgan S, Squire LR (1986) Memory impairment in monkeys following lesions limited to the hippocampus. Behav Neurosci 100:155–160

    Google Scholar 

  • Zola-Morgan S, Squire LR (1989) Amnesia in monkeys after lesions of the mediodorsal nucleus of the thalamus. Ann Neurol 17:558–564

    Google Scholar 

  • Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950–2967

    Google Scholar 

  • Zola-Morgan S, Squire LR, Amaral DG (1989) Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation. J Neurosci 9:1922–1937

    Google Scholar 

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  1. Department of Experimental Psychology, South Parks Road, OX1 3UD, Oxford, UK

    F. A. W. Wilson & E. T. Rolls

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  1. F. A. W. Wilson
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Wilson, F.A.W., Rolls, E.T. The effects of stimulus novelty and familiarity on neuronal activity in the amygdala of monkeys performing recognition memory tasks. Exp Brain Res 93, 367–382 (1993). https://doi.org/10.1007/BF00229353

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