The brain's orienting response (novelty P3) in patients with unilateral temporal lobe resections

Abstract

The brain’s orienting response is a biologically primitive, yet critical cognitive function necessary for survival. Though based on a wide network of brain regions, the lateral prefrontal cortex and posterior hippocampus are thought to play essential roles. Indeed, damage to these regions results in abnormalities of the novelty P3 or P3a, an event-related potential (ERP) sign of the orienting response. Like other ubiquitous markers of orienting, such as the galvanic skin response, the P3a habituates when novel events are repeated. Here, we assessed habituation of the P3a in patients who had undergone unilateral anteromedial resection of the medial temporal lobe (AMTL), including the entire hippocampus, for relief of pharmacologically intractable epilepsy. Eight left- and 8 right-AMTL patients and 16 age- and education-matched controls heard frequent standard tones, infrequent targets (requiring reaction times) and equally infrequent, unique novel, environmental sounds. The novel sounds repeated 2 blocks after their first presentation. In controls, novel repetition engendered a reduction in P3a amplitude, but this was not the case in either left- or right-AMTL patients. We conclude that bilaterally intact hippocampi are necessary for the brain to appreciate that a repetition of a novel sound has occurred, perhaps due to disruptions in ipsilateral hippocampal-prefrontal pathways and/or between the left and right hippocampi.

The effects of stimulus complexity on the preattentive processing of self-generated and nonself voices: An ERP study

“…On the basis of similar results, Graux et al (2013;Graux et al, 2015) proposed that enhanced processing resources are allocated to nonself voice stimuli when compared with one's own voice. Since the involuntary switch of attention is claimed to be a crucial biological process for survival (Friedman et al, 2001;Friedman, Nessler, Kulik, & Hamberger, 2012), a plausible interpretation for our findings, and for those reported by Graux et al (2013;Graux et al, 2015), is that the reorienting of attention toward an unexpected unfamiliar voice stimulus in the context of an unattended auditory environment may be more critical for survival than the detection of one's own voice. Fig.…”

Predictive coding of phonological rules in auditory cortex: A mismatch negativity study

“…The MMN and P3a results of the present study are also compatible with previous findings suggesting that large MMN and P3 responses indicate rule learning from auditory input (Mueller, Friederici, & Männel, 2012): attention switch indicated by P3a may, for example, enable the evaluation of the relevance of rule violation with respect to learning. Also results suggesting that hippocampal lesions reduce P3a to novel sounds imply that P3a may be linked with learning (Polich, 2007;Friedman, Nessler, Kulik, & Hamberger, 2011). In the case of strongly established native-language rules, however, the updating of their memory representations on the basis of occasional illegal stimuli is likely rejected, and thus no long-term learning occurs.…”

Markers of Novelty Processing in Older Adults Are Stable and Reliable

“…The neural and behavioral underpinnings of novelty processing have been investigated using functional imaging [PET and functional magnetic resonance imaging (fMRI; Tulving et al, 1996; Opitz et al, 1999; Downar et al, 2000, 2002; Kiehl et al, 2001a,b; Bunzeck and Düzel, 2006; Bunzeck et al, 2007, 2010, 2012; Strobel et al, 2008; Blackford et al, 2010)], magnetoencephalography (Bunzeck et al, 2009; Naeije et al, 2016), and especially high temporal resolution event-related potentials (ERPs) that are often measured during different kinds of oddball paradigms (Näätänen, 1990; Fabiani and Friedman, 1995; Daffner et al, 1998, 2001, 2003; Friedman et al, 2001; Polich and Comerchero, 2003; Schomaker and Meeter, 2014; Kaufman et al, 2016b). Although the N1, P2, and N2 ERP components have been shown to be elicited by novel stimuli (Courchesne et al, 1975; Beck et al, 1980; Chong et al, 2008; Riis et al, 2008; Friedman et al, 2011; Tarbi et al, 2011; Barry et al, 2013; Schomaker et al, 2014), the novelty P3 component remains the most commonly employed ERP marker of novelty processing (Friedman et al, 2001).…”