Ana B. Chica

Attentional routes to conscious perception.

The relationships between spatial attention and conscious perception are currently the object of intense debate. Recent evidence of double dissociations between attention and consciousness cast doubt on the time-honored concept of attention as a gateway to consciousness. Here we review evidence from behavioral, neurophysiologic, neuropsychological, and neuroimaging experiments, showing that distinct sorts of spatial attention can have different effects on visual conscious perception. While endogenous, or top-down attention, has weak influence on subsequent conscious perception of near-threshold stimuli, exogenous, or bottom-up forms of spatial attention appear instead to be a necessary, although not sufficient, step in the development of reportable visual experiences. Fronto-parietal networks important for spatial attention, with peculiar inter-hemispheric differences, constitute plausible neural substrates for the interactions between exogenous spatial attention and conscious perception.

Two cognitive and neural systems for endogenous and exogenous spatial attention

Orienting of spatial attention is a family of phylogenetically old mechanisms developed to select information for further processing. Information can be selected via top-down or endogenous mechanisms, depending on the goals of the observers or on the task at hand. Moreover, salient and potentially dangerous events also attract spatial attention via bottom-up or exogenous mechanisms, allowing a rapid and efficient reaction to unexpected but important events. Fronto-parietal brain networks have been demonstrated to play an important role in supporting spatial attentional orienting, although there is no consensus on whether there is a single attentional system supporting both endogenous and exogenous attention, or two anatomical and functionally different attentional systems. In the present paper we review behavioral evidence emphasizing the differential characteristics of both systems, as well as their possible interactions for the control of the final orienting response. Behavioral studies reporting qualitative differences between the effects of both systems as well as double dissociations of the effects of endogenous and exogenous attention on information processing, suggest that they constitute two independent attentional systems, rather than a single one. Recent models of attentional orienting in humans have put forward the hypothesis of a dorsal fronto-parietal network for orienting spatial attention, and a more ventral fronto-parietal network for detecting unexpected but behaviorally relevant events. Non-invasive neurostimulation techniques, as well as neuropsychological data, suggest that endogenous and exogenous attention are implemented in overlapping, although partially segregated, brain circuits. Although more research is needed in order to refine our anatomical and functional knowledge of the brain circuits underlying spatial attention, we conclude that endogenous and exogenous spatial orienting constitute two independent attentional systems, with different behavioral effects, and partially distinct neural substrates.

Dorsal and Ventral Parietal Contributions to Spatial Orienting in the Human Brain

Influential functional magnetic resonance imaging (fMRI)-based models have involved a dorsal frontoparietal network in the orienting of both endogenous and exogenous attention, and a ventral system in attentional reorienting to task-relevant events. Nonetheless, given the low temporal resolution and susceptibility to epiphenomenal activations of fMRI, such depictions remain highly debated. We hereby benefited from the high temporal resolution and causal power of event-related transcranial magnetic stimulation to explore the implications of key dorsal and ventral parietal regions in those two types of attention. We provide for the first time causal evidence of right intraparietal sulcus involvement in both types of attentional orienting, while we link the temporoparietal junction with the orienting of exogenous but not endogenous spatial attention.

Dissociating inhibition of return from endogenous orienting of spatial attention: Evidence from detection and discrimination tasks

In the present series of experiments, peripheral informative cues were used in order to dissociate endogenous and exogenous orienting of spatial attention using the same set of stimuli. For each block of trials, the cue predicted either the same or the opposite location of target appearance. Crucially, using this manipulation, both expected and unexpected locations could be either cued or uncued. If one accepts the hypothesis that inhibition of return (IOR) is an attentional effect that inhibits the returning of attention to a previously attended location (Posner & Cohen, 1984), one would not predict an IOR effect at the expected location, since attention should not disengage from the location predicted by the cue. Detection and discrimination tasks were used to examine any potential difference in the mechanism responsible for IOR as a function of the task at hand. Two major results emerged: First, IOR was consistently observed at the expected location, where, according to the traditional “reorienting” hypothesis, IOR is not supposed to occur. Second, a different time course of cueing effects was found in detection versus discrimination tasks, even after controlling for the orienting of attention. We conclude that IOR cannot be accounted for solely by the “reorienting of attention” hypothesis. Moreover, we argue that the observed time course differences in cueing effects between detection and discrimination tasks cannot be explained by attention disengaging from cues later in discrimination than in detection tasks, as proposed by Klein (2000). The described endogenous–exogenous dissociation is consistent with models postulating that endogenous and exogenous attentional processes rely on different neural mechanisms.

Effects of endogenous and exogenous attention on visual processing: An Inhibition of Return study

We investigate early (P1) and late (P3) modulations of event-related potentials produced by endogenous (expected vs. unexpected location trials) and exogenous (cued vs. uncued location trials) orienting of spatial attention. A 75% informative peripheral cue was presented 1000 ms before the target in order to study Inhibition of Return (IOR), a mechanism that produces slower responses to peripherally cued versus uncued locations. Endogenous attention produced its effects more strongly at later stages of processing, while IOR (an index of exogenous orienting) was found to modulate both early and late stages of processing. The amplitude of P1 was reduced for cued versus uncued location trials, even when endogenous attention was maintained at the cued location. This result indicates that the perceptual effects of IOR are not eliminated by endogenous attention, suggesting that the IOR mechanism produces a perceptual decrement on the processing of stimuli at the cued location that cannot be counteracted by endogenous attention.

The Spatial Orienting paradigm: how to design and interpret spatial attention experiments.

This paper is conceived as a guide that will describe the very well known Spatial Orienting paradigm, used to explore attentional processes in healthy individuals as well as in people suffering from psychiatric disorders and brain-damaged patients. The paradigm was developed in the late 1970s, and since then, it has been used in thousands of attentional studies. In this review, we attempt to describe, the paradigm for the naïf reader, and explain in detail when is it used, which variables are usually manipulated, how to interpret its results, and how can it be adapted to different populations and methodologies. The main goal of this review is to provide a practical guide to researchers who have never used the paradigm that will help them design their experiments, as a function of their theoretical and experimental needs. We also focus on how to adapt the paradigm to different technologies (such as event-related potentials, functional resonance imaging, or transcranial magnetic stimulation), and to different populations by presenting an example of its use in brain-damaged patients.

Spatial attention and conscious perception: the role of endogenous and exogenous orienting

Attention has often been considered to be a gateway to consciousness (Posner, Proceedings of the National Academy of Sciences of the United States of America, 91(16), 7398–7403, 1994). However, its relationship with conscious perception (CP) remains highly controversial. While theoretical models and experimental data support the role of attention in CP (Chica, Lasaponara, Lupiáñez, Doricchi, & Bartolomeo, NeuroImage, 51, 1205–1212, 2010; Dehaene, Changeux, Naccache, Sackur, & Sergent, Trends in Cognitive Sciences, 10, 204–211, 2006; Mack & Rock, Inattentional blindness,1998), recent studies have claimed that at least some forms of attention—endogenous or top-down spatial attention—are neither sufficient nor necessary for CP (Koch & Tsuchiya, Trends in Cognitive Sciences, 11, 16–22, 2007). In the present experiments, we demonstrate the importance of exogenously triggered attention for the modulation of CP. Weak or null effects were instead observed when attention was triggered endogenously. Our data are discussed in the framework of recent neuropsychological models (Dehaene et al., Trends in Cognitive Sciences, 10, 204–211, 2006), postulating that activity within reverberating frontoparietal networks, as colocalized with spatial--orienting systems, is the brain correlate of consciously processed information.

Two mechanisms underlying inhibition of return

Inhibition of return (IOR) refers to slower reaction times to targets presented at previously stimulated or inspected locations. Taylor and Klein (J Exp Psychol Hum Percept Perform 26(5):1639–1656, 2000) showed that IOR can affect either attentional/perceptual or motor processes, depending on whether the oculomotor system is in a quiescent or in an activated state, respectively. If the motoric flavour of IOR is truly non-perceptual and non-attentional, no IOR should be observed when the responses to targets are not based on spatial information. In the present experiments, we demonstrated that when the eyes moved to the peripheral cue and back to centre before the target appeared (to generate the motoric flavour), IOR was observed in detection tasks, for which the spatial location is an integral feature of the onset that is reported, but not in colour discrimination tasks, for which the outcome of a non-spatial perceptual discrimination is reported. When eye movements were prevented, both tasks showed robust IOR. We, therefore, conclude that the motoric flavour of IOR, elicited by oculomotor activation, does not affect attention or perceptual processing.

Cortical control of inhibition of return: Evidence from patients with inferior parietal damage and visual neglect

Inhibition of return (IOR) refers to slower reaction times to targets presented at previously stimulated or inspected locations. This phenomenon biases orienting towards novel locations and is functional to an effective exploration of the environment. Patients with right brain damage and left visual neglect explore their environment asymmetrically, with strong difficulties to orient attention to left-sided objects. We show for the first time a dissociation between manual and saccadic IOR in neglect. Our patients demonstrated facilitation, instead of inhibition, for repeated right-sided targets with manual responses, but normal IOR to right-sided targets with saccadic responses. All neglect patients had damage to the supramarginal gyrus in the right parietal lobe, or to its connections with the ipsilateral prefrontal cortex. We concluded that IOR with manual responses relies on fronto-parietal attentional networks in the right hemisphere, whose functioning is typically impaired in neglect patients. Saccadic IOR may instead depend on circuits less likely to be damaged in neglect, such as the retinotectal visual pathway.

Phasic auditory alerting improves visual conscious perception

Attention is often conceived as a gateway to consciousness (Posner, 1994). Although endogenous spatial attention may be independent of conscious perception (CP) (Koch Tsuchiya, 2007), exogenous spatial orienting seems instead to be an important modulator of CP (Chica, Lasaponara, Lupiáñez, Doricchi, & Bartolomeo, 2010; Chica, Lasaponara, et al., 2011). Here, we investigate the role of auditory alerting in CP in normal observers. We used a behavioral task in which phasic alerting tones were presented either at unpredictable or at predictable time intervals prior to the occurrence of a near-threshold visual target. We find, for the first time in neurologically intact observers, that phasic alertness increases CP, both objectively and subjectively. This result is consistent with evidence showing that phasic alerting can ameliorate the spatial bias exhibited by visual neglect patients (Robertson, Mattingley, Rorden, & Driver, 1998). The alerting network may increase the activity of fronto-parietal networks involved in top-down amplification required to bring a stimulus into consciousness (Dehaene, Changeux, Naccache, Sackur, & Sergent, 2006).