Adaptation in human visual cortex as a mechanism for rapid discrimination of aversive stimuli

Abstract

The ability to react rapidly and efficiently to adverse stimuli is crucial for survival. Neuroscience and behavioral studies have converged to show that visual information associated with aversive content is processed quickly and accurately and is associated with rapid amplification of the neural responses. In particular, unpleasant visual information has repeatedly been shown to evoke increased cortical activity during early visual processing between 60 and 120 milliseconds following the onset of a stimulus. However, the nature of these early responses is not well understood. Using neutral versus unpleasant colored pictures, the current report examines the time course of short-term changes in the human visual cortex when a subject is repeatedly exposed to simple grating stimuli in a classical conditioning paradigm. We analyzed changes in amplitude and synchrony of large-scale oscillatory activity across two days of testing, which included baseline measurements, 2 conditioning sessions, and a final extinction session. We found a gradual increase in amplitude and synchrony of very early cortical oscillations in the 20-35 Hz range across conditioning sessions, specifically for conditioned stimuli predicting aversive visual events. This increase for conditioned stimuli affected stimuluslocked cortical oscillations at a latency of around 60-90 ms and disappeared during extinction. Our findings suggest that reorganization of neural connectivity on the level of the visual cortex acts to optimize early perception of specific features indicative of emotional relevance.

Emotion-Associated Tones Attract Enhanced Attention at Early Auditory Processing: Magnetoencephalographic Correlates

“…Most neuroscientific affective conditioning studies investigated effects of associative learning during conditioning and/or postconditioning sessions only (Büchel et al, 1998;Pizzagalli et al, 2003;Phelps et al, 2004;Dolan et al, 2006;Stolarova et al, 2006;Keil et al, 2007). Relatively stronger processing of affective compared with neutral CS has consistently been interpreted as amplified processing of emotional stimuli.…”

“…We consider short-term plasticity in the auditory cortex in conjunction with top-down modulation by higher cognitive cortex structures as essential for this capacity. Associative learning is thought to induce short-term plasticity in auditory cortex (Edeline et al, 1993;Weinberger, 2004;Ohl and Scheich, 2005;Stolarova et al, 2006;Keil et al, 2007). The primary auditory cortex not only analyzes stimulus features but has been directly implicated in the storage of specific information about auditory experiences, among others, the behavioral relevance of auditory input (Weinberger, 2004).…”

“…In this form of associative learning, a formerly neutral stimulus (CS) comes to elicit a conditioned response (CR) previously associated with the presentation of an UCS alone after pairing CS and UCS in a contingent manner. Although studies both in animal and human research investigating differential affective conditioning typically use one conditioned stimulus per affective category (Quirk et al, 1995;Dolan et al, 2006;Stolarova et al, 2006;Keil et al, 2007), we here used a multitude of different CSs to be conditioned either with positive, negative, or neutral UCSs. We used this novel MultiCS-conditioning paradigm (cf.…”

“…The high temporal resolution offered by electroencephalography and magnetoencephalography (EEG/MEG) has been used to investigate the temporal dynamics of motivated attention in the visual system. Event-related potentials/magnetic fields (ERPs/ERMFs) measured in response to various types of affective pictorial stimuli were found to be modulated by motivated attention at distinct processing stages (Junghöfer et al, 2001;Schupp et al, 2004;Stolarova et al, 2006;Keil et al, 2007;Kissler et al, 2007), convergent to effects of directed attention Hillyard and Anllo-Vento, 1998;Martínez et al, 2001;Moratti et al, 2004;Ferrari et al, 2008).…”

Associative Learning Increases Trial-by-Trial Similarity of BOLD-MRI Patterns

“…Our study touches on four lines of neuroimaging research: (1) the investigation of human fear conditioning using traditional activation-based approaches (Büchel et al, 1998;LaBar et al, 1998); (2) research showing a link between the acquired emotional significance of a stimulus and more refined responses in perceptual cortices (Keil et al, 2007;Li et al, 2008;Padmala and Pessoa, 2008;Damaraju et al, 2009); (3) the application of MVPA to examine how the brain categorizes (Haxby et al, 2001;Polyn et al, 2005;Ethofer et al, 2009); and 4) the use of MVPA to assess learning-dependent changes (Li et al, 2009;Xue et al, 2010;Zhang et al, 2010). To begin with the last item, it has been fairly well established that learning how to discriminate nonemotional stimuli, such as Glass patterns, results in a more refined neural representation (i.e., a tuned response) for those particular stimuli (Li et al, 2009;Zhang et al, 2010).…”