Studies of human neuropathology have implicated the limbic system in the mediation of learning and memory processes. In accord with this result, our studies of unit activity in behaving animals have shown differentiation of neuronal responses to stimuli with varied associative significance. These effects occur in a triad of reciprocally interconnected limbic structures (the cingulate cortex, anteroventral thalamic nucleus [AVN], and hippocampal formation). Neurons in the deep cingulate cortical layers manifest discriminative firing in the early training stages, but the AVN and the superficial layers do not discriminate until discriminative behavior is well established. Similar relationships hold in the relative prefrontal corticothalamic system, but in this instance, the development of discriminative firing is accelerated, relative to the limbic triad. These results form the basis of a theory in which it is posited that the function of limbic forebrain in learning processes is the encoding and """"""""extraction"""""""" of que significance. The sequential character of the developing differential responses provided the rationale for the model's hypotheses about the causal relationships among the involved structures. Recent tests supported the model's hypotheses that the late discriminative code in the upper cortical layers originates in the AVN, and that the hippocampal formation (subiculum) exerts a tonic suppressive influence over neuronal firing in the cingulate cortex. This suppressive control, predicted by the model, provides a mechanisms to account for the behavioral hyperreactivity shown by animals with hippocampal damage. A major breakthrough has been the realization that the structures of the limbic triad produce an """"""""automatic"""""""" neural code relevant to the performance of well learned behavior, but not to its original acquisition. The analogous code in the prefrontal system is the """"""""leading edge"""""""" code subserving acquisition. Thus our studies identify separate neurobiological substrates for original discriminative acquisition, and for the maintenance of well learned behavior. Most importantly, the recent work indicates that selective removal of afferents yields selective neuronal effects in the recipient structures, and selective behavioral deficits. This general result supports the efficacy of our strategy for the functional analysis of interacting brain systems in relation to ongoing behavior. The proposed studies continue the analytic strategy by investigating the contributions to the significance coding process in the limbic triad made by afferents from the prefrontal system, the noradrenergic and basal forebrain cholinergic projections, the mammillothalamic projection, and possible influences of the pontine reticular formation.

Agency
National Institute of Health (NIH)
Institute
National Institute of Neurological Disorders and Stroke (NINDS)
Type
Research Project (R01)
Project #
5R01NS026736-08
Application #
3412716
Study Section
Neurosciences Research Review Committee (BPN)
Project Start
1982-08-21
Project End
1991-05-31
Budget Start
1989-06-01
Budget End
1990-05-31
Support Year
8
Fiscal Year
1989
Total Cost
Indirect Cost
Name
University of Illinois Urbana-Champaign
Department
Type
Schools of Arts and Sciences
DUNS #
041544081
City
Champaign
State
IL
Country
United States
Zip Code
61820
Talk, Andrew; Kang, Eunjoo; Gabriel, Michael (2004) Independent generation of theta rhythm in the hippocampus and posterior cingulate cortex. Brain Res 1015:15-24
Talk, Andrew; Kashef, Alireza; Gabriel, Michael (2004) Effects of conditioning during amygdalar inactivation on training-induced neuronal plasticity in the medial geniculate nucleus and cingulate cortex in rabbits (Oryctolagus cuniculus). Behav Neurosci 118:944-55
Smith, David M; Wakeman, Derek; Patel, Jay et al. (2004) Fornix lesions impair context-related cingulothalamic neuronal patterns and concurrent discrimination learning in rabbits (Oryctolagus cuniculus). Behav Neurosci 118:1225-39
Poremba, A; Gabriel, M (2001) Amygdalar efferents initiate auditory thalamic discriminative training-induced neuronal activity. J Neurosci 21:270-8
Duvel, A D; Smith, D M; Talk, A et al. (2001) Medial geniculate, amygdalar and cingulate cortical training-induced neuronal activity during discriminative avoidance learning in rabbits with auditory cortical lesions. J Neurosci 21:3271-81
Freeman Jr, J H; Gabriel, M (1999) Changes of cingulothalamic topographic excitation patterns and avoidance response incubation over time following initial discriminative conditioning in rabbits. Neurobiol Learn Mem 72:259-72
Taylor, C L; Freeman Jr, J H; Holt, W et al. (1999) Impairment of cingulothalamic learning-related neuronal coding in rabbits exposed to cocaine in utero: general and sex-specific effects. Behav Neurosci 113:62-77
Poremba, A; Gabriel, M (1999) Amygdala neurons mediate acquisition but not maintenance of instrumental avoidance behavior in rabbits. J Neurosci 19:9635-41
Kang, E; Gabriel, M (1998) Hippocampal modulation of cingulo-thalamic neuronal activity and discriminative avoidance learning in rabbits. Hippocampus 8:491-510
Hart, M; Poremba, A; Gabriel, M (1997) The nomadic engram: overtraining eliminates the impairment of discriminative avoidance behavior produced by limbic thalamic lesions. Behav Brain Res 82:169-77

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