Open and closed cortico-subcortical loops: A neuro-computational account of access to consciousness in the distractor-induced blindness paradigm☆
Introduction
The global workspace theory proposes that only a subset of stimuli available in the outside world enter consciousness to become globally available for task-control processes (Baars, 1988). In this view, the ‘global workspace’ refers to a high-level processing and storage system that allows for the interaction of different specialized brain areas (cf. Baars, 2005). But how are visual stimuli gated into this processing and storage system? In a model proposed by Dehaene, Sergent, and Changeux (2003), the amount of stimulus activation is the critical factor. Their model explains why salient, well visible or attended stimuli are particularly amenable to becoming consciously available. Cognitive influences on conscious access, in contrast, cannot be explained by this model.
The neuronal determinants of stimulus-driven and cognitive influences on access to consciousness can be measured through distinct neuro-psychological paradigms. Stimulus-driven influences, for instance, are prominent in the attentional blink paradigm, where subjects are asked to detect target stimuli in a rapid serial visual presentation (RSVP) stream. In this paradigm, targets that follow previous targets by about 180–450 ms cannot be reliably detected by subjects (Raymond, Shapiro, & Arnell, 1992). Cognitive influences on access to consciousness, in contrast, have been investigated using the distractor-induced blindness paradigm (Niedeggen et al., 2012, Sahraie et al., 2001). In this paradigm, two separate RSVP streams are presented. In a global RSVP stream containing target two (T2) visual stimuli are presented in an annulus centered on a fixation point. In a local stream, presented in the center of the global stream, target one (T1) is included. By instruction, T2-like stimuli that occur after T1 presentation are to be detected as targets, while T2-like stimuli presented before T1 serve as distractors. Effects of distractor-induced blindness (i.e., non-detection of targets because of previous distractors) can be observed if the time interval between T1 and T2 (stimulus onset asynchrony, SOA) is below approximately 300 ms (cf. Sahraie et al., 2001). This blindness effect does not rely on an interaction of the two targets, in contrast to the attentional blink paradigm (Shapiro, 1994), but on cognitive effects of target-like episodes (i.e., distractors) preceding the onset of T1 (Hesselmann et al., 2006, Sahraie et al., 2001): these target-like episodes have been shown to result in a frontal negativity, cumulatively inhibiting target perception, as shown in a recent event-related brain potential (ERP) study (Niedeggen et al., 2012). This top-down inhibitory effect of distractors, i.e., their power to decrease the probability of getting conscious access to T2, is a unique characteristic of distractor-induced blindness. The specific neuronal mechanisms of this inhibition, however, remain speculative.
Empirical studies have shown an involvement of the prefrontal cortex (PFC; Demerzti, Soddu, & Laureys, 2013), sensory cortical areas (for a review, see Rees, Kreiman, & Koch, 2002), cortico-thalamo-cortical loops (Demerzti et al., 2013, Llinás et al., 1998) and the basal ganglia (BG) in consciousness (e.g., Balkin et al., 2002, Christensen et al., 2006, Gray, 1995, Kjaer et al., 2002, Mhuircheartaigh et al., 2010, Palmiter, 2011). Overall, therefore, it appears likely that there exists a widespread cerebral substrate of consciousness, in which different structures may fulfill different functions. The BG in particular are likely to exert modulatory control over consciousness with their direct, indirect and hyperdirect pathways. This should not be understood as implying that the BG are necessary for phenomenal awareness. Rather, they can enhance, but also suppress activity within the thalamus and cortex via these pathways, potentially contributing to the distractor-induced inhibition of access to consciousness in the distractor-induced blindness paradigm.
We here focus on the involvement of cortico-BG-thalamic loops in conscious perception, extending on our previous proposal that the BG are fundamentally involved in making contents globally available by their control over thalamo-cortical loops (Trapp, Schroll, & Hamker, 2012). We implemented a novel neuro-computational model that explains how conscious perception may evolve from reverberation of activity in closed cortico-subcortical loops. The model further predicts that BG pathways can control access to these closed loops based on top-down context information, determining which pieces of information will be allowed to reverberate. In contrast to the model by Dehaene et al. (2003) outlined above, thereby, our model explains cognitive inhibitory influences on access to consciousness. Via interconnected open cortico-BG-thalamic loops, BG pathways are additionally proposed to determine how conscious perception influences response selection in the motor cortex.
Section snippets
Model architecture
Based on anatomical observations (Haber, 2003), the model consists of two interconnected cortico-BG-thalamic loops (Fig. 1): A closed ‘frontal’ loop determines which pieces of information become consciously available, while an open ‘motor’ loop determines response selection. Each modeled nucleus and cortical area contains a population of artificial neurons. These neurons are interconnected in accordance with anatomical evidence (cf. Bolam, Hanley, Booth, & Bevan, 2000) as presented in Fig. 2.
Conscious perception and response selection in the model
We propose that BG pathways can control access to consciousness. Via these pathways, cortical distractor and target stimuli bias information processing in closed cortico-subcortical loops. Before we address distractor-induced blindness in particular, Fig. 4 shows our model’s computations from cognitive to motor signals (wcontext → STN = 0.50, τact,dec = 50 ms, SOA = 0 ms) when faced with the distractor-induced blindness paradigm.
Presentation of a non-target fixation color activates model inputs that
Discussion
We propose a computational model that predicts conscious perception to arise from reverberating activity within closed cortico-subcortical loops. The model predicts that BG pathways control access to consciousness by either enhancing or suppressing gating of information into these closed loops. The model moreover predicts that the characteristics of information processing in BG pathways explain the phenomenon of distractor-induced blindness (cf. Sahraie et al., 2001): we show that the
Acknowledgments
This research was supported by a grant from the German Research Foundation (DFG HA2630/6-1) to Fred Hamker, within the Research Network “Neuro-Cognitive Mechanisms of Conscious and Unconscious Visual Perception” (PAK 270/1 and 2). The authors would like to thank Frederik Beuth (Department of Computer Science, Chemnitz University of Technology) for his generous technical support.
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This article is part of a special issue of this journal on Exploring the Visual (Un)conscious.
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C.E. and H.S. contributed equally.