Hippocampal networks habituate as novelty accumulates

Abstract

Novelty detection, a critical computation within the medial temporal lobe (MTL) memory system, necessarily depends on prior experience. The current study used functional magnetic resonance imaging (fMRI) in humans to investigate dynamic changes in MTL activation and functional connectivity as experience with novelty accumulates. fMRI data were collected during a target detection task: Participants monitored a series of trial-unique novel and familiar scene images to detect a repeating target scene. Even though novel images themselves did not repeat, we found that fMRI activations in the hippocampus and surrounding cortical MTL showed a specific, decrementing response with accumulating exposure to novelty. The significant linear decrement occurred for the novel but not the familiar images, and behavioral measures ruled out a corresponding decline in vigilance. Additionally, early in the series, the hippocampus was inversely coupled with the dorsal striatum, lateral and medial prefrontal cortex, and posterior visual processing regions; this inverse coupling also habituated as novelty accumulated. This novel demonstration of a dynamic adjustment in neural responses to novelty suggests a similarly dynamic allocation of neural resources based on recent experience.A fundamental task for organisms is to detect, learn about, and respond to change in the environment. Novelty responses in the brain signal environmental change and predict neural and behavioral adjustments to it; neural responses to novelty are thus a proxy for the salience of environmental change. Evidence from humans, nonhuman primates, and rodents points to a specialized brain system for the detection of novelty, centered around the hippocampus (HPC) and medial temporal lobe (MTL) memory system (Ranganath and Rainer 2003). It is now well documented that the HPC and MTL respond robustly to novel stimuli (Gabrieli et al. 1997;Jessen et al. 2002;Kohler et al. 2005;Bunzeck and Duzel 2006;Yassa and Stark 2008;Blackford et al. 2010;Howard et al. 2011). However, relatively little is known about how these responses are modulated by prior experience. In particular, how does a recent history rich with novel information influence MTL networks specialized for novelty processing?Other literature has described how prior exposure to biologically salient stimuli (or to a repeated feature) changes neural responses to future processing of those stimuli. Throughout the ventral visual stream, neural responses to repeated presentations of visually identical stimuli progressively decrease (Henson et al. 2003). Similarly, the amygdala and other structures implicated in fear processing habituate to cumulative exposure to trialunique stimuli that depict fear (Breiter et al. 1996;Wright et al. 2001;Fischer et al. 2003) or signal threat (Buchel et al. 1998;LaBar et al. 1998). Habituation has been proposed to be biologically adaptive: As a stimulus or feature is repeated, it provides less information about the environment, and demands fewer processing resources (Sokolov 1963;Rankin...

Reduced habituation in patients with schizophrenia

“…Our findings for hippocampal response to Different images were unexpected, as we anticipated there would be habituation to faces as a category (Gauthier et al, 2000) or to novelty itself (Murty et al, 2013). However, the presence of hippocampal discrimination is consistent with the comparator model of hippocampal function (Hasselmo and Wyble, 1997; Lisman and Grace, 2005).…”

Examining associations between psychosis risk, social anhedonia, and performance of striatum-related behavioral tasks.

“…Potentially, poor LIP in the PerMag group could reflect limbic striatum dysfunction that contributes to impaired novelty processing. However, although the Learned Irrelevance Paradigm is related to the limbic striatum, other parts of the brain (hippocampus & prefrontal cortex) also contribute to performance on these tasks (e.g., Murty, Ballard, Macduffie, Krebs, & Adcock, 2013; Young et al, 2005). Some issues for future PerMag research could be to measure functional brain activation on this task and also to examine other limbic striatum-related tasks to provide converging evidence for limbic striatum dysfunction.…”

A variable number of tandem repeats in the 3′‐untranslated region of the dopamine transporter modulates striatal function during working memory updating across the adult age span

“…This function is central to WM updating, which is the selective updating of old information with new incoming infor-mation (Murty et al, 2011). More recently, hippocampus and hippocampal-striatal interactions also have been implicated in learning processes (Schiffer et al, 2012;Brown & Stern, 2014;Murty et al, 2013). Hippocampal function is also regulated by dopamine signaling (Shohamy & Adcock, 2010).…”