Abstract
The purpose of this chapter is twofold: to describe the response properties of a class of reinforcement-related neurons (RRNs) in the basal forebrain of the monkey, and to provide a perspective on how processes of learning and memory influence these particular neurons. The basal forebrain is a complex region whose anatomical definition is being refined (see articles by Alheid, and Heimer in this book). In the context of this chapter, the term basal forebrain is restricted to the substantia innominata, the diagonal band of Broca, and a periventricular region adjacent to the walls of the third ventricle and anterior to the thalamus. These three regions share several common features: they contain cells that project to the cerebral cortex (Kievet and Kuypers, 1975; Mesulam et al., 1983), they receive afferent inputs from parahmbic regions of the cerebral cortex (Mesulam and Mufson, 1984; Russchen et al, 1985; Wilson and Rolls, 1990 a), and neurons with reinforcement-related activity are found throughout these three regions.
This is a preview of subscription content, log in via an institution to check access.
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
Aigner T., Mitchell S., Aggleton J.P., DeLong M., Struble R., Wenk G., Price D., and Mishkin M., 1984, Recognition deficit in monkeys following neurotoxic lesions of the basal forebrain. Soc. Neurosci. Abstr., 10: 116.11.
Bachevalier J., and Mishkin M., 1986, Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys. Behav. Brain Res., 20: 249.
Brown M.W., Wilson F.A.W., and Riches LP., 1987, Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory. Brain Res., 409: 158.
Brown D.A., 1983, Slow cholinergic excitation — a mechanism for increasing neuronal excitability. Trends in Neuroscience. 6:302.
Burton M.J., Rolls E.T., and Mora F., 1976, Effects of hunger on the responses of neurones in the lateral hypothalamus to the sight and taste of food, Exp. Neurol. 5: 668.
Damasio A.R., Graff-Radford N.R., Eslinger P.J., Damasio H., and Kassal N., 1985, Amnesia following basal forebrain lesions. Arch. Neurol. 42: 263.
DeLong M.R., 1971, Activity of pallidal neurons during movement, J. Neurophysiol 34: 414.
Flicker C., Ferris S.H., Crook T., Bartus R.T., and Reisberg B., 1985, Cognitive function in normal aging and early dementia, in: “Senile Dementia of the Alzheimer type”, Traber J., Gispen W.H., eds, Springer-Verlag, Berlin, pp. 269.
Friedman H.M., and Allen N., 1969, Chronic effects of complete limbic lobe destruction in man. Neurology. 19: 679.
Funahashi S., Bruce C.J., and Goldman-Rakic P.S., 1989, Mnemonic coding of visual space in the monkey’s dorsolateral prefrontal cortex. J. Neurophysiol. 61: 331.
Gascon G.G., and Gilles F., 1973, Limbic dementia. J. Neurol Neurosurg. Psychiat., 36: 421.
Grant S.J., and Aston-Jones G., 1986, Discharge properties of cortically projecting nucleus basalis neurons in behaving animals. Soc Neurosci. Abstr., 12:158.
Horel J. A., 1978, The neuroanatomy of amnesia: a critique of the hippocampal memory hypothesis. Brain. 101: 403.
Horel J.A., Pytko-Joiner D.E., Voytko M., and Salsbury K., 1987, The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behav. Brain Res., 23: 29.
Kievet J., and Kuypers H.G.J.M., 1975, Basal forebrain and hypothalamic connections to prefrontal and parietal cortex in the rhesus monkey. Science. 187: 660.
Kopelman M.D., and Com T.H., 1988, Cholinergic ‘blockade’ as a model for cholinergic depletion. Brain 111: 1079.
Lamour Y., Dutar P., Jobert A., and Dykes R.W., 1988, An iontophoretic study of single somatosensory neurons in rat granular cortex serving the limbs: a laminar analysis of glutamate and acetylcholine effects on receptive-field properties, J. Neurophysiol. 60: 725.
Leonard C.M., Rolls E.T., Wilson F.A.W. and Baylis G.C., 1985, Neurons in the amygdala of the monkey with responses selective for faces. Behav. Brain Res., 15: 159.
Mesulam M-M., Mufson EJ., Levey A.I., and Wainer B.H., 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.
Mesulam M-M., and Mufson E.J., 1984, Neural inputs into the nucleus basalis of the substantia innominata (CH4) in the rhesus monkey. Brain, 107: 257.
Mesulam M-M., Volicer L., Marquis J.K., Mufson E.J., and Green R.C., 1986, Systematic regional differences in the cholinergic innervation of the primate cerebral cortex: distribution of enzyme activities and some behavioral implications. Ann. Neurol., 19: 144.
Mishkin M., A memory system in the monkey, 1982, Phil. Trans. Roy. Soc. Lond., B298: 89.
Mitchell S.J., Richardson R.T, Baker F.H., and Belong M.R., 1987, The primate nucleus basalis of Meynert: neuronal activity related to a visuomotor ti-acking task, Exp. Brain Res., 68: 506.
Mora P., Rolls E.T., and Burton M.J., 1976, Modulation during learning of the responses of neurones in the lateral hypothalamus to the sight of food. Exp. Neurol., 53: 508.
Murphy J.P., and Gellhom E., 1945, The influence of hypothalamic stimulation on cortically-induced movements and on action potentials of the cortex, J. Neurophysiol. 8: 339.
Murray E.A., and Mishkin M., 1984, Severe tactual as well as visual memory deficits follow combined removals of the amygdala and hippocampus in monkeys. J. Neurosci., 4: 2580
Murray E.A., and Mishkin M., 1986, Visual recognition in monkeys following rhinal cortical ablations combined with either amygdalectomy or hippocampectomy. J. Neurosci., 6: 1991.
Olton D.S., Becker J.T., and Handelman G.E., 1979, Hippocampus, space and memory. Behav. Brain Sciences 2: 313.
Pearson R.C.A., Esiri M.M., Hioms R.W., Wilcock G.K., and Powell T.P.S., 1985, Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer’s disease, Proc. Nat. Acad. Sci. U.S.A., 82: 4531.
Richardson R. T., and DeLong M.R., 1986, Nucleus basalis of Meynert neuronal activity during a delayed response task in monkey, Brain Res., 399: 364.
Richardson R. T., and DeLong M.R., 1987, Tonically active nucleus basalis neurons in the awake monkey project to cerebral cortex, Soc. Neurosci. Abstr., 13: 1027.
Richardson R. T., and DeLong M.R., 1990, Context dependent responses of primate nucleus basalis neurons during a go/no go task, J. Neurosci. 10: 2528.
Riches LP., Wilson F.A.W. and Brown M.W., 1990, The effects of visual stimulation and memory on neurones of the primate hippocampal formation and the neighbouring parahippocampal gyrus and inferior temporal cortex of the primate (submitted for publication).
Ridley R.M., Baker H.F., Drewett B., and Johnson J.A., 1985, Effects of ibotenic acid lesions of the basal forebrain on serial reversal learning in marmosets, Psychopharmacol., 86: 438.
Rigdon G.C., and Pirch J.H., 1986, Nucleus basalis involvement in conditioned neuronal responses in the rat frontal cortex. J. Neurosci., 6: 2535.
Robbins T.W., Everitt B.J., Ryan C.N., Marston H.M., Jones G.H., and Page K.J., 1989a, Comparative effects of quisquaüc and ibotenic acid-inducing lesions of the substantia innominata and globus pallidus on the acquisition of a conditional visual discrimination: differential effects on cholinergic mechanisms. Neuroscience. 28: 337.
Robbins T.W., Everitt B.J., Marston H.M., Wilkinson J., Jones G.H., and Page K.J., 1989b, Comparative effects of ibotenic acid and quisqualic acid-inducing lesions of the substantia innominata on attentional function in the rat: futher implications for the role of cholinergic neurons of the nucleus basalis in cognitive processes. Beh. Brain Res., 35: 221.
Roberts A.C., Robbins T.W., Everitt B.J., Jones G.H., Sirkia T.E., Wilkinson J., and Page K., 1990, The effects of excitotoxic lesions of the basal forebrain on the acquistion, retention and serial reversal of visual discrimination in marmosets. Neuroscience. 34: 311.
Rolls E.T., Burton M.J., and Mora P., 1976, Hypothalamic neuronal responses associated with the sight of food. Brain Res., 11: 53.
Rolls E.T., Perrett D.I., Caan A.W., and Wilson F.A.W., 1982, Neuronal responses related to visual recognition, Brain. 105: 611.
Russchen F.T., Amaral D.G., and Price J.L., 1985, The afferent connections of the substantia innominata in the monkey, macaca fascicularis, J. Comp. Neurol. 242: 1.
Semba K., Reiner P.B., McGeer E.G., and Fibiger H.C., 1989, Brainstem projecting neurons in the rat basal forebrain: neurochemical, topographical and physiological distinctions from cortically projecting cholinergic neurons. Brain Res. Bull. 22: 501.
Schultz W., and Romo R., 1990, Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. J. Neurophvsiol., 63; 607.
Sillito A.M., and Kemp J. A., 1983, Cholinergic modulation of the functional organisation of the cat visual cortex, Brain Res., 289:143.
Stuss D.T., and Benson D.F., 1986, “The Frontal Lobes”, Raven Press, New York.
Thorpe S.J., Rolls B.T., and Maddison S., 1983, The orbitofrontal cortex: neuronal activity in the behaving monkey, Exp. Brain Res., 49: 93.
Travis R.P., and Sparks D.L., 1969, Unitary responses and discrimination leaming in the squirrel monkey: the globus pallidus, Physiol. Behav., 3: 187.
Voytko M.L., 1985, Cooling orbitofrontal cortex disrupts matching-to-sample and visual discrimination leaming in monkeys. Physiol. Psvchol. 13: 219.
Voytko M.L., Olton D.S., Richardson R.T., Wenk D.L. and Price J.L., 1990, Lack of memory impairment following basal forebrain lesions in monkeys. Soc. Neurosci. Abstr., 16: 258.9.
Whitehouse P.J., 1990, Pathology in basal forebrain in dementia: implication for treatment. The Neurotransmitter, 3: 3, Loyola University Chicago Medical Center.
Whitehouse P.J., Price A.W., Struble R.G., Clark A.W., Coyle J.T., and DeLong M.R., 1982, Alzheimer’s disease and senile dementia: loss of neurons in the basal forebrain. Science. 215: 1237.
Whitlock D.G., and Nauta W.J.H., 1956, Subcortical projections from the temporal neocortex in macaca mulatta. J. Comp. Neurol, 106: 184.
Wilson F.A.W., 1989, Cortical and subcortical structures involved in recognition memory: physiological and anatomical studies. Int. J. Neurol. 21–22.
Wilson F.A.W., M.W. Brown and LP. Riches, 1988, Neuronal activity in the inferomedial temporal cortex compared to that in the hippocampal formation: implications for amnesia of medial temporal lobe origin, in: “Cellular Mechanisms of Conditioning and Behavioural Plasticity”, C.D. Woody, D.L. Alkon and J.L. McGaugh, eds, Plenum Press, New York, pp. 313.
Wilson F.A.W., and Goldman-Rakic P.S., 1989, Effect of spatial and color cues on delay-related neuronal responses in prefrontal cortex. Soc. Neurosci. Abstr., 20: 33.5
Wilson F.A.W., and Goldman-Rakic P.S., 1990, Viewing preferences of rhesus monkeys related to memory for complex pictures, colours and faces (in preparation).
Wilson F.A.W., LP. Riches, and M.W. Brown, 1990, Medial temporal neuronal activity related to behavioural responses during the performance of memory tasks by primates. Behav. Brain Res, (in press).
Wilson F.A.W., and Rolls E.T., 1990a, Neuronal responses related to novelty and familiarity of visual stimuli in the substantia innominata, diagonal band of Broca and Priventricular region of the primate basal forebrain. Exp. Brain Res., 80: 104.
Wilson F.A.W., and Rolls E.T., 1990b, Neuronal responses related to reinforcement in the primate basal forebrain. Brain Res., 509: 213.
Wilson F.A.W., and Rolls E.T., 1990c, Leaming and memory is reflected in the responses of reinforcement-related neurons in the primate basal forebrain. J. Neurosci., 10: 1254.
Wilson F.A.W., and Rolls E.T., 1990d, The primate amygdala and reinforcement: a dissociation between rule-based and associatively-mediated memory reflected in neuronal activity (submitted for publication).
Zola-Morgan S., Squire L.R., and Amaral D.G. (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.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1991 Plenum Press, New York
About this chapter
Cite this chapter
Wilson, F.A.W. (1991). The Relationship between Learning, Memory and Neuronal Responses in the Primate Basal Forebrain. In: Napier, T.C., Kalivas, P.W., Hanin, I. (eds) The Basal Forebrain. Advances in Experimental Medicine and Biology, vol 295. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-0145-6_13
Download citation
DOI: https://doi.org/10.1007/978-1-4757-0145-6_13
Publisher Name: Springer, Boston, MA
Print ISBN: 978-1-4757-0147-0
Online ISBN: 978-1-4757-0145-6
eBook Packages: Springer Book Archive