A theory of cerebral learning regulated by the reward system

Hypothetical mechanisms of the neocorticohippocampal system are presented. Neurophysiological and neuroanatomical findings concerning the system are integrated to demonstrate how animals associate sensory stimuli with rewarding actions: (1) cortical plasticity regulated by cholinergic/noradrenergic inputs from the hypothalamic reward system reinforces association connections between the most activated columns in the cortex; (2) the repetitive reinforcement forms association pathways connecting sensory cortical columns activated by the stimuli with motor cortical columns producing the rewarding actions; (3) after the pathways are formed, the cortex is capable of temporarily memorizing the stimuli by producing long-term potentiation through the cortico-hippocampal circuits; and (4) the memory allows the cortex to extend correct association pathways even in an environment where sensory stimuli rapidly change. A mathematical model of parts of the nervous system is presented to quantitatively examine the mechanisms. Membrane characteristics of single neurons are given by the Hodgkin-Huxley electric circuit. According to anatomical data, neural circuits of the neocortico-hippocampal system are composed by connecting populations of the model neurons. Computer simulation using physiological data concerning ion channels demonstrates how the mechanisms work and how to test the hypotheses presented.

[1]  J. Eccles The Physiology of Synapses , 1964, Springer Berlin Heidelberg.

[2]  B. Gordon,et al.  The role of norepinephrine in plasticity of visual cortex , 1988, Progress in Neurobiology.

[3]  A. Keller,et al.  Long-term potentiation of thalamic input to the motor cortex induced by coactivation of thalamocortical and corticocortical afferents. , 1991, Journal of neurophysiology.

[4]  R. Llinás,et al.  Ionic basis for the electro‐responsiveness and oscillatory properties of guinea‐pig thalamic neurones in vitro. , 1984, The Journal of physiology.

[5]  R. Llinás,et al.  Electrophysiological properties of guinea‐pig thalamic neurones: an in vitro study. , 1984, The Journal of physiology.

[6]  G. Ahlsén,et al.  Excitation of perigeniculate neurones via axon collaterals of principal cells , 1982, Brain Research.

[7]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  R. W. Guillery,et al.  Retinotopic organization within the thalamic reticular nucleus demonstrated by a double label autoradiographic technique , 1977, Brain Research.

[9]  A. Sefton,et al.  Mode of termination of afferents from the thalamic reticular nucleus in the dorsal lateral geniculate nucleus of the rat , 1980, Brain Research.

[10]  M. Dubin,et al.  Elimination of action potentials blocks the structural development of retinogeniculate synapses , 1986, Nature.

[11]  B. L. Ginsborg THE PHYSIOLOGY OF SYNAPSES , 1964 .

[12]  G. Ahlsén,et al.  Corticofugal projection to perigeniculate neurones in the cat. , 1983, Acta physiologica Scandinavica.

[13]  G. Lynch,et al.  Intracellular injections of EGTA block induction of hippocampal long-term potentiation , 1983, Nature.

[14]  G. Kass-simon,et al.  Excitatory and Inhibitory Interactions in the Opener Muscle of Lobster Claws , 1989 .

[15]  G. V. Hoesen,et al.  The parahippocampal gyrus: New observations regarding its cortical connections in the monkey , 1982, Trends in Neurosciences.

[16]  E. Kumamoto,et al.  Long-term potentiations in vertebrate synapses: a variety of cascades with common subprocesses , 1990, Progress in Neurobiology.

[17]  C. Koch,et al.  The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus , 2004, Experimental Brain Research.

[18]  T. Teyler,et al.  The hippocampal memory indexing theory. , 1986, Behavioral neuroscience.

[19]  A. Scheibel,et al.  The organization of the nucleus reticularis thalami: a Golgi study. , 1966, Brain research.

[20]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

[21]  James L Olds Drives and reinforcements : behavioral studies of hypothalamic functions / by James Olds , 1977 .

[22]  N Ishizuka [Structural organization of hippocampal cortex]. , 1989, No to shinkei = Brain and nerve.

[23]  H. Sakata,et al.  Functional Organization of a Cortical Efferent System Examined with Focal Depth Stimulation in Cats , 1967 .

[24]  G. Ahlsén,et al.  Mutal inhibition between perigeniculate neurones , 1982, Brain Research.

[25]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[26]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[27]  E. G. Jones,et al.  Some aspects of the organization of the thalamic reticular complex , 2004, The Journal of comparative neurology.

[28]  A. Ichikawa,et al.  Cerebral mechanism for reward-mediated learning: A mathematical model of neuropopulational network plasticity , 1990, Biological Cybernetics.

[29]  Shun-ichi Amari,et al.  Characteristics of Random Nets of Analog Neuron-Like Elements , 1988, IEEE Trans. Syst. Man Cybern..

[30]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  A. Luria The Working Brain , 1973 .

[32]  F. H. C. Crick,et al.  Certain aspects of the anatomy and physiology of the cerebral cortex , 1986 .