The central role of the prefrontal cortex in directing attention to novel events

Abstract

The physiological basis for the striking decrease of attention to novel events following frontal lobe injury is poorly understood. In this study, event-related potentials (ERPs) were recorded from patients with frontal lobe damage and matched subjects, who controlled the duration of viewing of background, novel and target stimuli. Frontal lobe patients did not differ from normal controls in terms of age, education, estimated IQ or mood. However, they were judged to be more apathetic as measured by self-report and informants' ratings. Patients with frontal lobe damage exhibited markedly reduced amplitude of the novelty P3 response and the duration of viewing of novel stimuli. In contrast, injury to the frontal lobes had a limited impact on P3 amplitude and behavioural responses (viewing duration and reaction time) to target stimuli. A strong correlation was found between measures of apathy and both attenuated P3 amplitude and viewing duration in response to novel but not target stimuli. Differences in amplitude of the novelty P3 response explained a large portion of the variance associated with duration of viewing of novel stimuli. After controlling for the influence of P3 amplitude, there was no association between frontal lobe injury and reduced viewing of novel stimuli. The results of this study suggest that frontal lobe damage leads to diminished visual attention to novel events through its disruption of neural processes underlying the novelty P3 response. These processes appear to regulate the allocation of attentional resources and early exploratory behaviours, and are not limited to immediate orienting responses. Damage to the frontal lobes may prevent the generation of a signal which indicates that a novel event in the environment requires additional attention due to its potential behavioural significance. The disruption of these processes is likely to contribute to the apathy observed in patients after injury to the frontal lobes.

Compensatory neural activity distinguishes different patterns of normal cognitive aging

“…The difference between cognitively high and average performers on tests of attention and executive functioning was found to be marginally smaller for young subjects than middle-age subjects. There is evidence that a person's frontal-executive system may play a central role in mediating the novelty P3 component (Daffner et al, 2000b). Furthermore, as suggested by theories about cognitive reserve, eliciting electrophysiological differences between cognitively high and average performing young subjects may require a much more demanding task than the one employed in the current study.…”

“…The experimental procedures used were analogous to the ones described in prior reports (Daffner et al, 2000b;Daffner et al, 2006b). Two hundred and fifty line drawings, white on black background, were presented in 5 blocks of 50, each at the center of a high-resolution computer monitor.…”

Novelty Enhancements in Memory Are Dependent on Lateral Prefrontal Cortex

“…For example, evidence from studies using ERPs, depth electrodes in humans, and single-unit studies in monkeys suggests that the PFC plays an important role in novelty detection (Knight, 1984;Halgren et al, 1998;Daffner et al, 2000;Matsumoto et al, 2007). In addition, evidence from lesion, ERP, and functional magnetic resonance imaging studies indicate that both the PFC and MTL are thought to constitute critical components of a distributed novelty detection network (Knight, 1996(Knight, , 1997McCarthy et al, 1997;Knight and Scabini, 1998;Strange and Dolan, 2001;Yamaguchi et al, 2004).…”

“…For example, event-related potential (ERP) findings from patients with focal lesions or implanted electrodes suggest that regions in medial temporal lobes (MTL) and prefrontal cortex (PFC) constitute critical components of this network (Knight, 1984(Knight, , 1996Halgren et al, 1998;Knight and Scabini, 1998;Daffner et al, 2000). In addition, some ERP evidence suggests that the right lateral PFC and particularly the dorsolateral PFC (DLPFC) may be important for novelty processing (Alexander et al, 1995;Knight and Scabini, 1998;Daffner et al, 2000). However, because memory was not typically measured in these studies, they do not reveal whether MTL and PFC regions are critical for producing stimulus novelty effects in memory.…”

Updating P300: An integrative theory of P3a and P3b

“…Debener et al, 2005;Escera et al, 1998;Goldstein et al, 2002). ERP and fMRI studies suggest that a frontal attention mechanism governs neural responsivity to novelty (Daffner et al, 2000a(Daffner et al, , 2000b(Daffner et al, , 2000cSuwazono et al, 2000), thereby implying top-down control (Bledowski et al, 2004a;Dien et al, 2004;Kiehl et al, 2005;Opitz et al, 1999;Opitz, 2003). Attentional resources used to maintain memory items in parietal regions may result from response organization produced by bottom-up processing (Conroy and Polich, 2007;Nieuwenhuis et al, 2005;Verleger et al, 2005).…”