ReviewOrienting of spatial attention and the interplay between the senses
Introduction
In everyday life our brain is bombarded with a multitude of sensory signals. Some of these signals are relevant and require in-depth processing, while others need filtering out. Selection and filtering operations are two main functions of the attention control system (Desimone and Duncan, 1995, Kastner and Ungerleider, 2001). There are many rules that guide and constrain the attentional selection process. One critical factor is the behavioural relevance of the input: if a sensory signal is useful to the achievement of our current goals, then that specific input will receive in-depth processing. This emphasises the notion that internal (endogenous) goals are important determinants of the selection process. However, the selection mechanism should also be flexible, enabling switching to new goals when the circumstances require doing so. Accordingly, unexpected external signals must also gain some access to the selection control system (stimulus-driven control, Corbetta et al., 2008).
Here, I will examine the interplay between endogenous and stimulus-driven attention control in the context of spatial orienting. Space is an interesting element for attentional selection for several reasons. First, our motor systems generally operate toward one spatial location at a time. We can direct our gaze toward a single position at a time, and we typically reach out to grasp an object at a single position at a time (or maximum two, for bimanual reaching). Thus, the motor systems have to continuously commit to specific locations, implementing a drastic form of spatial selection. Second, spatial selectivity is a pervasive characteristic of single neurons (i.e., the receptive field of a neuron) and well-organised maps of space can be found almost everywhere in the brain (Gross and Graziano, 1995). Third, brain damage, particularly to right hemisphere, can cause relatively specific spatial deficits (Vallar and Perani, 1986, Karnath et al., 2004). Also, space provides us with a picture of the external world that we can access in an intuitive manner. Just try to imagine shuffling around different parts of a photograph: you may get an excellent work of modern art, but not much else.
Another interesting characteristic of spatial representations is that these can be invariant across the senses. Albeit with different levels of precision in the different sensory modalities, e.g., very high for vision but lower for audition, we can often register the position of an object or an event using different senses. The spatial co-localisation of multiple inputs in different sensory modalities can facilitate the detection of an external object (e.g., a car approaching that we can both see and hear) aiding identification and speeding up reactions. Spatial alignment is considered a key determinant for combining multisensory signals (Stein and Meredith, 1993, Meredith and Stein, 1996; see also Stein and Meredith, 1993, for review). Accordingly, space can be used not only to select or filter out sensory input, but it also plays a role for the integration of these signals (multisensory integration).
In this review I will first examine neural substrates and constraints governing the functioning of the attentional system in the visual modality. I will discuss how “external” (stimulus-driven) signals and “internal” (endogenous) task-related goals jointly contribute to the spatial orienting of attention. In the second part, I will turn to studies of multisensory spatial attention. I will argue that the integration of spatial representations across sensory modalities provides a substrate onto which attentional selection can take place. In multisensory contexts, selection and attention control can operate via several different functional/anatomical pathways, highlighting distinctive mechanisms beyond those present in the case of unimodal visuo-spatial attention.
Section snippets
Neural basis of visuo-spatial attention control
Spatial attention in humans has been examined extensively using neuropsychological and neuroimaging methods. One of the most popular paradigms to investigate spatial attention functions is the cueing procedure first proposed by Posner et al. (1980). This entails the presentation of a cue that indicates one of the two hemifields. After a brief delay, a target stimulus is presented either at the cued location (valid trial) or on the opposite side (invalid trial). In one version of this paradigm (
Interplay between endogenous and stimulus-driven visuo-spatial attention
The activation of vFP is typically associated with stimulus-driven reorienting of attention, when a stimulus is presented outside the focus of attention (e.g., as for invalidly cued targets, Arrington et al., 2000, Vossel et al., 2006). However, the fact that subjects have to discriminate and respond to these targets is likely to also entail some form of endogenous processing. For example, the recognition of the target stimulus and the mapping the sensory input into a correct motor response
Multisensory attention
Most behavioural and electrophysiological studies on spatial attention considered only one modality at the time (mostly vision or audition); but a growing body of evidence demonstrates that stimuli in different sensory modalities can interact, jointly contributing to spatial attention orienting. Many studies have now shown that directing attention to one location in one modality can facilitate the processing of stimuli presented at the same location, but in a different modality (Driver and
Multisensory integration and exogenous spatial attention
The proposal that spatial information is shared across multisensory (e.g., dFP) and unisensory areas (e.g., visual cortex, see Fig. 5b) suggests a link between spatial attention control and multisensory integration of space. However, multisensory integration is generally thought to occur in a fully stimulus-driven manner, while the multisensory imaging results described in the previous section concern situations of endogenous, voluntary attention control. The question arises of whether
Revised models of spatial attention control
These findings call for a further extension of “site-source” models of attention control, which need to take into account the particular status of multisensory stimuli. In conditions of pure visual attention, the functional coupling between sensory areas in occipital cortex and the vFP (TPJ) is subject to inhibitory influences, likely to originate from dorsal regions (Fig. 5a, see also Corbetta et al., 2008). This inhibition is released only when the incoming visual signals are task-set
Summary and future directions
The investigation of attention control in multisensory situations led to several new observations, which require some revision of current models of attention control. These should take into account that: (1) most attention control regions in frontal and parietal cortex are multimodal and combine information arising from the different senses; (2) crossmodal interactions can affect activity in sensory-specific areas and they can do so in a spatially specific manner; (3) conditions involving
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