Hippocampal control of cingulate cortical and anterior thalamic information processing during learning in rabbits

Abstract

Past studies of the neural determinants of discriminative avoidance conditioning in rabbits have fostered a theoretical model that describes the interactive functioning of the cingulate cortex (Brodmann's Areas 24 and 29), the anterior ventral and medial dorsal thalamic nuclei (AVN and MDN) and the hippocampus. Here we test hypotheses of the model concerning the influence of the hippocampus on cortical and thalamic information processing. The rabbits learned to perform locomotory conditioned responses (CRs) in an activity wheel in response to an acoustic (pure tone) positive conditional stimulus (CS+). A shock unconditional stimulus (US) was given 5 s after CS+ onset, but locomotion during the CS+ - US interval prevented the US. The rabbits also learned to ignore a second tone (a negative conditional stimulus, CS-) of different auditory frequency than the CS+, that did not predict the US. Multi-unit activity and intracranial macropotentials were recorded in the cingulate cortex and the AVN during acquisition, overtraining, extinction, reacquisition and reversal training. Data were obtained in intact rabbits and in rabbits with bilateral lesions of the subicular complex, the origin of projections of the hippocampal formation to the cingulate cortex and AVN. In addition, the activity in the AVN was recorded in a separate group of rabbits with posterior cingulate cortical (Area 29) lesions. Subicular and Area 29 lesions were associated with an enhancement of the training-induced CS+ elicited neuronal response in the AVN. The frequency of CRs was enhanced in animals with subicular lesions. CS elicited unit responses in the cingulate cortices were attenuated in rabbits with subicular lesions. Both of the lesions were associated with significantly increased amplitudes of the CS elicited average cortical and thalamic macropotentials. These results suggested the following conclusions: subiculocortical afferents provide an enabling influence that is essential for CS elicited excitation in the cingulate cortex; the cingulate cortical excitatory response in intact animals exerts a limiting influence on the activity in the AVN; the enhanced AVN neuronal response in rabbits with lesions is due to the absence of the limiting influence and it contributes to the increased CR frequency in those animals. It is hypothesized that the hippocampus via subiculocortical projections, governs the flow of CR-inducing thalamocortical excitatory volleys. This governance determines the timing of CR output. The results of hippocampal processing of contextual information acting through the subiculocortical projection determines the moment most appropriate for the CR.

Mamillothalamic tract transection blocks anterior thalamic training- induced neuronal plasticity and impairs discriminative offidance behavior in rabbits

“…Bilateral electrolytic subicular complex lesions enhanced AV thalamic discriminative training-induced activity Lesi ons and Anterior Thalamic Unit Activity (Gabriel et al, 1987) indicating that the subicular afferents are not essential for training-induced activity production but may instead provide an inhibitory modulation of the training-induced activity.…”

“…Experimental damage to subicular and cingulate cortical neurons that project to limbic thalamus did not attenuate but rather enhanced the limbic thalamic training-induced activity (Gabriel et al, 1986(Gabriel et al, , 1987. Lesions of the limbic thalamic nuclei abolished training-induced activity and virtually all tone-elicited activity in cingulate cortex (Gabriel et al, 1989).…”

Amygdalar Lesions Block Discriminative Avoidance Learning and Cingulothalamic Training-Induced Neuronal Plasticity in Rabbits

“…The thalamic training-induced neuronal plasticity does not depend on cerebral cortical afferents, because lesions in projecting cingulate cortical and hippocampal formation areas did not interfere with, indeed they enhanced, the development of the thalamic plasticity (Gabriel et al, 1987.…”

Evidence for extrahippocampal involvement in place learning and hippocampal involvement in path integration

“…Gabriel et al (1987) suggested that cingulate cortex is a repository for learned responses and that the hippocampus is involved in updating those responses. Thus, according to this view, initial learning may involve the cortex, whereas updating a learned response requires participation of the hippocampus.…”