Cortical Contributions to Higher-Order Conditioning: A Review of Retrosplenial Cortex Function

Abstract

In higher-order conditioning paradigms, such as sensory preconditioning or second-order conditioning, discrete (e.g., phasic) or contextual (e.g., static) stimuli can gain the ability to elicit learned responses despite never being directly paired with reinforcement. The purpose of this mini-review is to examine the neuroanatomical basis of high-order conditioning, by selectively reviewing research that has examined the role of the retrosplenial cortex (RSC) in sensory preconditioning and second-order conditioning. For both forms of higher-order conditioning, we first discuss the types of associations that may occur and then review findings from RSC lesion/inactivation experiments. These experiments demonstrate a role for the RSC in sensory preconditioning, suggesting that this cortical region might contribute to higher-order conditioning via the encoding of neutral stimulus-stimulus associations. In addition, we address knowledge gaps, avenues for future research, and consider the contribution of the RSC to higher-order conditioning in relation to related brain structures.

Keywords: associative learning; higher-order conditioning; retrosplenial cortex; second-order conditioning; sensory preconditioning.

FIGURE 1

Schematic of higher-order conditioning procedures. The figure depicts typical experimental conditioning for sensory preconditioning (A) and second-order conditioning (B), which are contrasted with control conditions (not shown). Discrete stimuli can be presented either serially (top row) or simultaneously (middle row). Higher-order conditioning of contextual stimuli is presented in the bottom row. Contexts are operationally defined as the static background stimuli provided by conditioning apparatus, and typically differ with respect to visual, tactile and olfactory characteristics. In the figure, contexts are distinguished by color and background.

FIGURE 2

A simplified schematic depicting retrosplenial connections with cortical and subcortical regions. The connectomic diagram is centered around retrosplenial cortex and does not include the complex interactions between all regions. V1, primary visual cortex; V2, secondary visual cortex; A1, primary auditory cortex; A2, secondary auditory cortex.