In this investigation, we probed pulvinar responses with the goal of characterizing how they are linked to affective processing and stimulus visibility during resource-poor conditions. Pulvinar responses were evaluated in two ways, first in terms of mean responses (via ANOVAs) and in terms of trial-by-trial response fluctuations (via logistic regression). The mean-response analysis revealed that pulvinar responses were not influenced by affective significance (CS+ vs. CS−) per se, but that they were closely tied to perception (hit vs. miss). Notably, a Conditioning by Perceptual Decision interaction was detected for the left pulvinar (because of greater differential hit vs. miss responses during the CS+ relative to the CS− condition). The trial-by-trial analysis revealed that moment-to-moment fluctuations in response magnitude followed trial-by-trial detection performance, and thereby closely tracked target visibility. Logistic regression slopes differed as a function of affective significance (CS+ vs. CS−) for the left pulvinar, a result that paralleled the Conditioning by Perceptual Decision interaction observed in the ANOVA (note that logistic regression slopes are based on considering both hit and miss trials).
The logistic regression analysis summarized how trial-by-trial fluctuations in response strength were linked to behavioral performance. Another aspect of the link between pulvinar responses and behavior was investigated by considering the influence of affective significance on mean responses. Participants with larger differential responses during hit trials (CS+ vs. CS−) exhibited a correspondingly larger behavioral improvement. These results, which were observed in both left and right hemispheres, are consistent with the notion that improvements in behavioral performance were linked to how affective significance enhanced evoked responses in the pulvinar during hit trials.
Some of our findings differed between the left and right pulvinar. The significance of the differences is unclear at the moment, but it is noteworthy that both hemispheres exhibited brain–behavior correlations (Figures C,F). In addition, across individuals, trial-by-trial fluctuations in evoked responses in both hemispheres tracked stimulus visibility during the CS+ condition (Figures B,D).
In our previous report, the comparison between CS+ and CS− miss
trials did not reveal significant differential responses in the amygdala or visual cortex (Lim et al., 2009
). Contrary to suggestions of stronger automaticity of emotion-laden stimuli, the affective nature of a stimulus itself did not guarantee robust differential responses, which indicates that affective perception is under the control of attentional mechanisms during temporal “bottleneck” conditions (Stein et al., 2010
) – in addition to during spatial manipulations of attention (Pessoa, 2005
). Because of these prior results and their theoretical importance, here we probed responses during miss
trials, too. No significant differences were observed in the left or right pulvinar. These results are of particular importance in the context of the putative subcortical pathway, as one of its central properties is that it conveys information rapidly and independently of attention and awareness.
Our results are thus inconsistent with a “strongly automatic” view of pulvinar function, one that is often encountered in the context of affective processing. Broadly speaking, the interpretation of findings of the attentional blink in general (i.e., not only in affective paradigms) is complex because both attention and awareness are involved in the paradigm (Bowman and Wyble, 2007
; Shapiro, 2009
; Martens and Wyble, 2010
), and it is becoming increasingly clear that even though attention and awareness are related, they may also be partially dissociated (Lau and Passingham, 2006
; Koch and Tsuchiya, 2007
). For instance, attention can affect perceptual processing and behavioral performance in the absence of awareness (Kentridge et al., 2004
; Bahrami et al., 2007
). Here, although pulvinar responses tracked stimulus visibility, it was not possible to disentangle the contributions of the pulvinar to attention and awareness processes.
In the present study, as well as in our previous report (Lim et al., 2009
), we focused on specific regions of interest given a priori
questions of theoretical and empirical importance. Accordingly, we do not claim that the present findings are specific to the pulvinar. Indeed, many of the present results paralleled those observed in the amygdala and visual cortex, where trial-by-trial fluctuations in response magnitude closely tracked behavioral performance. More broadly, we anticipate that other brain regions may exhibit similar patterns of results, for instance attentional regions in frontal and parietal cortices given that responses in these regions have been shown to be closely linked to task performance (Pessoa et al., 2002
; Marois and Ivanoff, 2005
It could be argued that a role for the pulvinar in subcortical affective processing is not adequately tested in the present study because of the choice of stimuli employed. In other words, because the detection of the second target involved a house vs. building discrimination, detailed form processing may have been involved – and would presumably not be conveyed subcortically. Note, however, that our stimuli were selected so as to be easily discriminable. Specifically, on the one hand, building stimuli involved images with a clear vertical elongation; houses, on the other hand, lacked this type of asymmetry. Consistent with the suggestion that the categories did not require detailed visual information to be told apart, low spatial-frequency versions of our stimuli are easily discriminated from each other (see Figure for an example). Nevertheless, because of the stimuli adopted here, the present study is unable to assess the suggestion that the purported subcortical pathway is involved in the processing of “biologically prepared” stimuli (Ohman and Mineka, 2001
). Along related lines, the present study employed a differential conditioning procedure that is more complex than some of the conditioning procedures employed in the animal literature (LeDoux, 1996
). Accordingly, it would be of value to test variants of the procedure employed here that utilized simpler conditioning procedures.
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 (more ...)
In the present study, behaviorally, the detection of the second target occurred more frequently during the CS+ compared to the CS− condition. What are the circuits by which affective significance influenced perception? Although our study does not answer this question, we suggest the following working hypothesis. In our task, the effect of emotion necessitates the categorization of buildings and houses, a process that likely depends on territories in ventral occipitotemporal cortex. Information from anterior aspects of the ventral visual stream is then conveyed to the amygdala (Amaral et al., 1992
) – thus completing a “feedforward sweep.” The amygdala is suggested, then, to play a key role in determining the affective value of incoming stimuli (including houses and buildings in our task), and in modulating visual activation based on this assessment (Vuilleumier et al., 2004
More generally speaking, what is the role of the pulvinar in emotion? Studies by Ward and colleagues help illuminate potential roles of the pulvinar during affective processing. For instance, a complete unilateral loss of the pulvinar led to a severe deficit in a patient's ability to recognize fearful expressions shown in the contralesional field (Ward et al., 2007
). In an earlier study, viewing complex unpleasant images impaired a subsequent simple (neutral) visual task in controls, but not in a patient with pulvinar damage (Ward et al., 2005
) – compatible with the idea that the unpleasant stimulus did not garner additional resources in the patient, which would have interfered with performance, as in the controls.
Taken together with the broader literature on the role of the pulvinar in attention and awareness, we propose the following working hypothesis for the function of the pulvinar in emotion. Broadly speaking, the role of the pulvinar in emotion is integrative (see also Shipp, 2003
; Ward et al., 2007
). In particular, the medial pulvinar is interconnected with large portions of the cortex, including parietal, frontal, insular, orbital, and cingulate cortices (Grieve et al., 2000
; Shipp, 2003
) – in addition to being connected to the amygdala (Jones and Burton, 1976
; Romanski et al., 1997
). As part of thalamocortical loops with all these diverse cortical territories, the medial pulvinar is thus well positioned to influence the flow of information processing in the brain according to a stimulus's biological significance (note that the medial pulvinar needs to be distinguished from the inferior pulvinar, the latter being more closely associated with visual functions; see Grieve et al., 2000
; Shipp, 2003
and Figure ). In particular, when weak and/or brief visual stimuli have affective significance, cortico-pulvino-cortical circuits may act such that signals are coordinated and amplified in a manner that will enhance their behavioral impact (Figure ). In the present study, the pulvinar's contribution to affective processing was discernible in several ways. As stated previously, at the average response level, increased response to hit
trials during the CS+ condition relative to the CS− condition was correlated with behavioral performance. Furthermore, in the left pulvinar, a Conditioning by Perceptual Decision interaction was observed, reflecting a larger differential response to hits
for affectively significant (CS+) stimuli. The same relationship was also evident at the trial-by-trial level, as the slopes of the logistic fits were significantly steeper for CS+ stimuli (in the left pulvinar). Our findings thus reveal important interactions between emotional content and perception in the pulvinar.
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 (more ...)
In conclusion, our results do not support a passive role of the pulvinar in affective processing, as often invoked in the context of the subcortical-pathway hypothesis (for further discussion, see Pessoa, 2005
). Instead, the pulvinar appears to be involved in mechanisms that are closely linked to attention and awareness, a role that may be particularly important during the processing of affectively significant stimuli.