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. 2010 Sep 24;4:64.
doi: 10.3389/fnhum.2010.00064. eCollection 2010.

Pulvinar and Affective Significance: Responses Track Moment-to-Moment Stimulus Visibility

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Free PMC article

Pulvinar and Affective Significance: Responses Track Moment-to-Moment Stimulus Visibility

Srikanth Padmala et al. Front Hum Neurosci. .
Free PMC article

Abstract

Research on emotion has considered the pulvinar to be an important component of a subcortical pathway conveying visual information to the amygdala in a largely "automatic" fashion. An older literature has focused on understanding the role of the pulvinar in visual attention. To address the inconsistency between these independent literatures, in the present study, we investigated how pulvinar responses are involved in the processing of affectively significant stimuli and how they are influenced by stimulus visibility during attentionally demanding conditions. Subjects performed an attentional blink task during fMRI scanning involving affectively significant (CS+) and neutral stimuli (CS-). Pulvinar responses were not influenced by affective significance (CS+ vs. CS-) per se. Instead, evoked responses were only modulated by affective significance during hit trials, but not during miss trials. Importantly, moment-to-moment fluctuations in response magnitude closely tracked trial-by-trial detection performance, and thereby visibility. This relationship was only reliably detected during the affective condition. Our results do not support a passive role of the pulvinar in affective processing, as invoked in the context of the subcortical-pathway hypothesis. Instead, the pulvinar appears to be involved in mechanisms that are closely linked to attention and awareness. As part of thalamocortical loops with diverse cortical territories, we argue that the medial pulvinar is well positioned to influence information processing in the brain according to a stimulus's biological significance. In particular, when weak and/or brief visual stimuli have affective significance, cortico-pulvino-cortical circuits may act to coordinate and amplify signals in a manner that enhances their behavioral impact.

Keywords: attention; attentional blink; conditioning; emotion; subcortical pathway.

Figures

Figure 1
Figure 1
Experimental paradigm. (A) Affective significance was manipulated during an initial learning phase. In this example, building stimuli were paired with mild shock 50% of the time, while house stimuli were not paired with shock. (B) Subjects performed the attentional blink task, which involved reporting two target stimuli (T1: face; T2: scene) among a stream containing 18 distractors. T2 stimuli could be a CS+ (building; top panel), a CS− (house; bottom panel) or a distractor stimulus (not shown).
Figure 2
Figure 2
Pulvinar responses. (A–C) Left pulvinar responses. (A) Average time-courses of evoked responses in the left pulvinar ROI as a function of experimental condition. Evoked responses of individual trials were based on the average of time points at 6 and 8 s post trial onset (see shaded area) – i.e., 4–6 following T2 presentation (indicated schematically via the inset containing the house stimulus). (B) Bar plots showing the same data as in (A) based on the average of time points 6 and 8 s post trial onset. (C) Scatter plot illustrating the correlation between evoked responses in the left pulvinar ROI and behavioral performance across participants (percent correct difference). (D–F) Right pulvinar responses. Parts (D–F) correspond to parts (A–C), respectively. No error bars are included in (B,E) because our interest was on within-subject differences and, in particular, the within-subject interaction pattern.
Figure 3
Figure 3
Trial-by-trial analysis of hit vs. miss trials. (A,B) Left pulvinar. (A) Logistic regression analysis of evoked responses in the left pulvinar ROI as a function of affective significance (CS+ and CS−) for a sample individual. The slope of the logistic fit indicates the strength of the predictive effect. For clarity, only binned data for the CS+ condition are shown (black dots). (B) Mean logistic slopes across individuals for the left pulvinar. (C,D) Right pulvinar. Parts (C,D) correspond to parts (A,B), respectively. Error bars in (B,D) are 95% confidence intervals around the mean.
Figure 4
Figure 4
Frequency content of T2 stimuli. Original and low spatial frequency content of typical house and building T2 stimuli used in this study. It is apparent that house and building stimuli can be discriminated easily based on low spatial frequency information alone. In the low-pass images, building stimuli exhibit a clear vertical elongation; houses, on the other hand, lacked this type of asymmetry.
Figure 5
Figure 5
Affective significance and the pulvinar. When weak, though affectively significant stimuli are encountered (as shown in the inset), interactions between the medial (Med) pulvinar and several brain regions important for the determination of “biological value” influence the flow of information processing, such that signals related to such items are amplified, thus leading to increased behavioral effects. Note that only some of the connections between the amygdala, orbitofrontal cortex (OFC), cingulate, and insula are provided (shown in purple). In contrast to the medial pulvinar, which is largely “associational,” the inferior (Inf) pulvinar is bidirectionally connected with striate and extra-striate cortex, and is thus much more “visual”.

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