Changes of Cingulothalamic Topographic Excitation Patterns and Avoidance Response Incubation over Time Following Initial Discriminative Conditioning in Rabbits

doi:10.1006/nlme.1998.3896

Neurobiology of Learning and Memory

Volume 72, Issue 3, November 1999, Pages 259-272

https://doi.org/10.1006/nlme.1998.3896 Get rights and content

Abstract

Neurons in particular layers of cingulate cortex and in limbic thalamic nuclei exhibit peak firing rates in response to a positive conditional stimulus (CS+) in particular stages of discriminative learning. A given area is maximally activated by the CS+ in the initial, an intermediate, or a late stage of behavioral acquisition, and activation in all of the areas diminishes as training continues after the peak of activation occurs. Thus, the topographic distribution of activation in these areas depends on the stage of behavioral acquisition. The present study determined whether the acquisition-related changes of the topographic distributions of peak firing rates in CS-elicited activity are driven exclusively by the repetition of conditioning trials (i.e., practice) or may occur as well with the passage of time, similar to putative processes of memory consolidation. Multiunit activity was recorded in cingulate cortex and in the anterior dorsal (AD), anterior ventral (AV), and medial dorsal (MD) thalamic nuclei as rabbits learned to step in response to a warning tone (CS+) to prevent a scheduled foot-shock, and to ignore a different tone (CS−) not predictive of foot-shock. The rabbits received two training sessions, S1 and S2. S2 followed S1 immediately in one group of rabbits and after 48 h in a different group. Significant neuronal discharge increments occurred from S1 to S2 in the 48-h group but not in the 0-h group, for the areas (posterior cingulate cortex, AV thalamic nucleus) that previously showed only late-stage activation. Significant discharge increments occurred from S1 to S2 in the 0-h group but not in the 48-h group in areas (anterior cingulate cortex, the AD, and MD thalamic nuclei) that previously exhibited early stage activation. These results indicate that the trial-driven topographic distribution changes also occur with the passage of time after limited initial training. It is suggested that the trial-driven and time-related changes may have a common functional relevance concerning memory consolidation.

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¹: John Freeman is now at the Department of Psychology, The University of Iowa, Seashore Hall, Iowa City, IA 52242.

²: This research was supported by NIH Grants NS26736 and NS36591, NSF Grant BIR95-04842, and a grant from the University of Illinois Research Board to M.G. Correspondence concerning this article should be addressed to Michael Gabriel, Beckman Institute, University of Illinois, 405 North Mathews Avenue, Urbana IL 61801. Fax: (217) 244-5180; E-mail: [email protected].

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Standard Research ReportChanges of Cingulothalamic Topographic Excitation Patterns and Avoidance Response Incubation over Time Following Initial Discriminative Conditioning in Rabbits

Abstract

Behavioral Biology

Behavioural Brain Research

Behavioural Brain Research

Brain Research

Current Opinion in Neurobiology

Neuroscience and Biobehavioural Reviews

Behavioural Brain Research

Short-term and long-term verbal memory: A positron emission tomography study

Proceedings of the National Academy of Science USA

A device for motor conditioning of small animals

Science

Multiple unit recording: Technique, interpretation, and experimental applications

Extended temporal gradient for the retrograde and anterograde amnesia produced by ibotenate entorhinal cortex lesions in mice

Journal of Neuroscience

Trial sequence of changed unit activity in auditory system of alert rat during conditioned response acquisition and extinction

Journal of Neurophysiology

A metachromatic stain for neural tissue

Stain Technology

A rapid method for locating intracerebral electrode tracks

Stain Technology

Context-specific multi-site cingulate cortical, limbic thalamic, and hippocampal neuronal activity during concurrent discriminative approach and avoidance training in rabbits

Journal of Neuroscience

Lesions of the entorhinal cortex disrupt behavioral and neuronal responses to context change during extinction of discriminative avoidance behavior

Experimental Brain Research

Effects of intersession delay and training level on avoidance extinction and intertrial behavior

Journal of Comparative and Physiological Psychology

Functions of anterior and posterior cingulate cortex during avoidance learning in rabbits. The prefrontal cortex: Its structure, function and pathology

Progress in Brain Research

Discriminative avoidance learning: A model system

Interaction of laminae of the cingulate cortex with the anteroventral thalamus during behavioral learning

Science

Standard Research Report
Changes of Cingulothalamic Topographic Excitation Patterns and Avoidance Response Incubation over Time Following Initial Discriminative Conditioning in Rabbits