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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 basal forebrain

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This study examined correlates of memory processes in neuronal activity recorded from the substantia innominata, the diagonal band of Broca and the periventricular region or the basal forebrain of monkays performing recognition and/or visual discrimination tasks. Two types of neurons were found that responded differentially to stimuli on the basis of their novelty or their familiarity. Neurons (5/572) in the periventricular region rostral to the thalamus and caudal to the anterior commissure responded to familar stimuli with increases in firing rate. Neurons in the substantia innominata (16/ 1058) and in the diagonal band (14/489) responded maximally to novel stimuli, with smaller responses to repeared presentations of these stimuli. The properties of these two types of neurons were similar in three respects: (1) the magnitude of the differential response to novel and familiar presentations of stimuli were largest for stimuli presented on successive trials, and were attenuated for stimuli that had not been seen for some intervening trials; (2) both types of neurons responded to highly familiar stimuli as if they were novel if they had not been recently seen; (3) both types responded to two- and three-dimensional stimuli; and were recorded in rhesus monkeys trained on the recognition tasks and in untrained cynomolgus monkeys. An injection of HRP into the periventricular region of one monkey resulted in retrograde labeling of ventromedial regions of the prefrontal, cingulate and temporal cortices, of the amygdala, medial thalamus, supramammillary region of the midbrain. These data indicate that information about the novelty, familiarity or recency of presentation of visual stimuli is reflected in the responses of some basal forebrain neurons. Neurons in the substantia innominata and diagonal band of Broca could not be distinguished using the battery of applied tests, suggesting functional mechanisms common to both regions. The results of the anatomical experiment suggest that ventromedial limbic cortical and subcortical regions projecting to or through the periventricular region may be important for the transmission of information about visual stimuli and for memory function.

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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 (1984) Projections of the amygdala to the thalamus in the cynomolgus monkey. J Comp Neurol 222:56–68

    Google Scholar 

  • Aigner T, Mitchell S, Aggleton JP, Delong M, Strubble R, Wenk G, Price D, Mishkin M (1984) Recognition deficit in monkeys following neurotoxic lesions of the basal forebrain. Soc Neurosci Abstr 10:116.11

    Google Scholar 

  • Albert M, Moss M (1984) The assessment of memory disorders in patients with Alzheimer's disease. In: Squire LR, Butters N (eds) Neuropsychology of memory. Guildford Press, New York, pp 236–246

    Google Scholar 

  • Alexander MP, Freedman M (1984) Amnesia after anterior communicating artery aneurysm rupture. Neurology 34:752–757

    Google Scholar 

  • Angelergues R (1969) Memory disorders in neurological disease. In: Vinken PJ, Bruyn GW (eds) Handbook of clinical neurology, Vol 3. American Elsevier, New York, pp 268–292

    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 

  • 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 

  • Damasio AR, Graff-Radford NR, Eslinger PJ, Damasio H, Kassal N (1985) Amnesia following basal forebrain lesions. Arch Neurol 42:263–271

    Google Scholar 

  • Dean RL, Bartus RT (1985) Animal models of geriatric cognitive dysfunction: evidence for an important cholinergic involvement. In: Traber J, Gispen WH (eds) Senile dementia of the Alzheimer type. Springer, Berlin, pp 269–282

    Google Scholar 

  • Flicker C, Ferris SH, Crook T, Bartus RT, Reisberg B (1985) Cognitive function in normal aging and early dementia. In: Traber J, Gispen WH (eds) Senile dementia of the Alzheimer type. Springer, Berlin, pp 269–282

    Google Scholar 

  • Friedman HM, Allen N (1969) Chronic effects of complete limbic lobe destruction in man. Neurology 19:679–689

    Google Scholar 

  • Gascon GG, Gilles F (1973) Limbic dementia. J Neurol Neurosurg Psychiat 36:421–430

    Google Scholar 

  • Geffen G, Walsh A, Simpson D, Jeeves M (1980) Comparison of the effects of transcortical and transcallosal removal of intraventricular tumours. Brain 103:773–788

    Google Scholar 

  • Hanker JS, Yates PE, Meltz CB, Rustioni AJ (1977) A new specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochem J 9:789–792

    Google Scholar 

  • Hedreen JC, Struble RG, Whitehouse PJ, Price DL (1984) Topography of the magnocellular basal forebrain system in human brain. J Neuropath Exp Neurol 43:1–21

    Google Scholar 

  • Horel JA (1978) The neuroanatomy of amnesia: a critique of the hippocampal memory hypothesis. Brain 101:403–445

    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 

  • Humphrey NK (1972) ‘interest’ and ‘pleasure’: two determinants of a monkey's visual preferences. Perception 1:395–416

    Google Scholar 

  • Huppert FA, Piercy M (1978) The role of trace strength in recency and frequency judgements by amnesic and control subjects. QJ Exp Psych 30:347–354

    Google Scholar 

  • Jones EG, Burton H, Saper CB, Swanson LW (1976) Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J Comp Neurol 167:385–420

    Google Scholar 

  • Jürgens U, Müller-Preuss P (1977) Convergent projections of different limbic vocalisation areas in the squirrel monkey. Exp Brain Res 29:75–83

    Google Scholar 

  • Kievit J, Kuypers HGJM (1975) Basal forebrain and hypothalmic connections to prefrontal and parietal cortex in the rhesus monkey. Science 187:660–662

    Google Scholar 

  • Leichnetz GR, Astruc J (1977) The course of some prefrontal corticofugals to the pallidum, substantia innominata and amygdaloid complex in monkeys. Exp Neurol 54:104–109

    Google Scholar 

  • Luria AR, Homskaya ED, Blinkov SM, Critchley McD (1967) Impaired selectivity of mental processes in association with a lesion of the frontal lobe. Neuropsychologia 5:105–117

    Google Scholar 

  • Mahut H, Zola-Morgan S, Moss M (1982) Hippocampal resections impair associative learning and recognition memory in the monkey. J Neurosci 2:1214–1229

    Google Scholar 

  • Mair WGP, Warrington EK, Weiskrantz L (1979) Memory disorder in Korsakoff's psychosis. Brain 102:749–783

    Google Scholar 

  • Mesulam M-M, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata) and hypothalamus in the rhesus monkey. J Comp Neurol 214:170–197

    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 

  • 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. Phil Trans R Soc Lond B298:89–95

    Google Scholar 

  • Murray EA, Mishkin M (1984) Severe tactual as well as visual memory deficits follow 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 

  • Nichelli P, Baraldi A, Cappelli G (1982) Hypernaetremic thirst deficiency and memory disorders following hypothalamic lesions. Arch Psychiat Nervenkr 231:459–470

    Google Scholar 

  • Parent A, DeBellefeuille L (1982) Organisation of efferent projections from the internal segment of the globus pallidus in the primate revealed by the fluorescence retrograde labeling method. Brain Res 245:201–213

    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

    Google Scholar 

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

    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 

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

    Google Scholar 

  • Squire LR, Moore RY (1979) Dorsal thalamic lesion in a noted case of chronic memory dysfunction. Ann Neurol 6:503–506

    Google Scholar 

  • Talland GA, Sweet WH, Ballantine Jr, TH (1967) Amnesic syndrome with anterior communication artery aneurysm. J Nerv Ment Dis 145:179–192

    Google Scholar 

  • Taren JA (1965) Anatomical pathways related to the clinical findings in aneurysms of the anterior communicating artery J Neurol Neurosurg Psychiat 28:228–234

    Google Scholar 

  • Van Buren JM, Borke RC (1972) The mesial temporal substratum of memory: anatomical studies in three individuals. Brain 95:599–632

    Google Scholar 

  • Veazey RB, Amaral DG, Cowan WM (1982) The morphology and connections of the posterior hypothalamus in the cynomolgus monkey (Macaca fascicularis). 2. Efferent connections. J Comp Neurol 207:135–156

    Google Scholar 

  • Volpe BT, Hirst W (1983) The characterisation of two patients with amnesia following the rupture and repair of anterior communicating artery aneurysm. J Neurol Neurosurg Psychiat 46:704–709

    Google Scholar 

  • Wallesch CW, Kornhuber HH, Kollner C, Haas HC, Hufnagl JM (1983) Language and cognitive deficits from medial and dorsolateral frontal lobe lesions. Arch Psychiat Nervenkr 233:279–296

    Google Scholar 

  • Whitehouse PJ, Price AW, Struble RG, Clark AW, Coyle JT, DeLong MR (1982) Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215:1237–1239

    Google Scholar 

  • Whitlock DG, Nauta WJH (1956) Subcortical projections from the temporal neocortex in Macaca mulatta. J Comp Neurol 106:184–207

    Google Scholar 

  • Williams M, Penneybacker J (1954) Memory disturbances in third ventricle tumours. J Neurol Neurosurg Psychiat 17:115–123

    Google Scholar 

  • Wilson FAW, Rolls ET, Yaxley S, Thorpe SJ, Williams GV, Simpson SJ (1984) Responses of neurons in the basal forebrain of the behaving monkey. Soc Neurosci Abstr 10:37.8

    Google Scholar 

  • Wilson FAW (1985) Neuronal activity related to novelty, familiarity and reinforcement. Ph D thesis. University of Oxford

  • 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, 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 Press, New York, pp 313–328

    Google Scholar 

  • Winocur G, Oxbury S, Roberts R, Agnetti A, Davis C (1984) Amnesia in a patient with bilateral lesions to the thalamus. Neuropsychologia 22:123–143

    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 

  • Woody CD, Kim E, Berthier NE (1983) Effect of hypothalamic stimulation on unit responses recorded from neurons of sensorimotor cortex of awake cats during conditioning. J Neurophysiol 49:780–791

    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 

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Wilson, F.A.W., Rolls, E.T. 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 basal forebrain. Exp Brain Res 80, 104–120 (1990). https://doi.org/10.1007/BF00228852

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