Abstract
Several competing theories on the mechanisms underlying attentional control have emerged over the years that, despite their substantial differences, all emphasize the importance of hemispheric asymmetries. Transcranial magnetic stimulation (TMS) has proven particularly successful in teasing them apart by selective perturbation of the dorsal and ventral fronto-parietal network. We here critically review the TMS literature and show that hemispheric asymmetries within the dorsal attention network differ between parietal and frontal cortex. Specifically, posterior parietal cortex seems to be characterized by a contralateral bias of each hemisphere and competition between them. In contrast, the right frontal eye field seems to be involved in shifting attention toward both hemifields, whereas left frontal eye field is only involved on shifting attention toward the contralateral hemifield. In the light of presented evidence, we propose to revise the functional-anatomical model originally proposed by Corbetta and Shulman (2011, 2002) and introduce a hybrid model of hemispheric asymmetries in attentional control
. Introduction
The voluntary control of attention allows prioritizing those aspects of incoming sensory information that are relevant to us. It therefore constitutes a vital prerequisite for goal-directed behavior and enables us to effectively deal with the abundance of sensory information entering the brain. Already during the beginnings of psychology and neuroscience, the importance of this selection mechanism has been recognized (James, 1890), and there is a wealth of studies investigating the effects of attention on behavior, the functional mechanisms of attentional control, and the underlying neuronal processes (Carrasco, 2011, Corbetta and Shulman, 2002, Desimone and Duncan, 1995, Reynolds and Chelazzi, 2004, Reynolds and Heeger, 2009 and Ungerleider and Kastner, 2000).
Similar to the discovery of many other brain functions, neuropsychological findings regarding the behavioral consequences of brain damage have provided first evidence for the involvement of certain brain areas in attentional control and have inspired theories on their functional properties. Especially a neurological syndrome called spatial hemineglect has been very influential. Various models of spatial neglect have been proposed over the years and they have shaped theories on spatial attention control until the present day ( Bisiach et al., 1996, Halligan et al., 2003, Milner and McIntosh, 2005, Posner et al., 1987 and Robertson, 2001). Spatial hemineglect is caused by lesions to frontal, parietal, or sub-cortical structures and is characterized by impaired attentional processing within the space contralateral to the lesion's location ( Bartolomeo et al., 2012, Corbetta et al., 2005, Duncan et al., 1999, Karnath et al., 2002, Karnath and Rorden, 2012 and Mesulam, 1999). Most importantly, the phenomenon of spatial neglect is more common and severe after right hemisphere damage than after left hemisphere damage, suggesting a functional asymmetry of the mechanisms underlying spatial attention ( French Collaborative Study Group on Assessment of Unilateral Neglect, 2004 and Suchan et al., 2012). Based on this observation, two competing theories of spatial attention have originally emerged, namely Heilman's hemispatial theory and Kinsbourne's opponent processor model, both accounting for this asymmetry but proposing very different mechanisms ( Heilman and Abell, 1980, Heilman and Valenstein, 1979 and Kinsbourne, 1977). Despite the many advances in cognitive neuroscience in the last decades, it has been rather difficult to differentiate between these two models with the majority of existing methods. However, transcranial magnetic stimulation (TMS) has proven quite successful in teasing them apart, indeed revealing functional asymmetries between the left and right hemisphere with regard to spatial attention control. With the debate far from being settled, Corbetta and Shulman proposed a functional-anatomical model, strongly supported by neuroimaging data, that offered yet another explanation for the pre-dominance of spatial neglect after right hemisphere damage ( Corbetta and Shulman, 2002 and Corbetta and Shulman, 2011). And again, TMS seems to be well-suited to test specific predictions derived from that model.
Here, we first present the three competing models of spatial attention control and lay out their explanatory approach to spatial hemineglect. We then review several lines of research, all based on the application of TMS in healthy volunteers, that have produced critical insights into the mechanisms underlying attentional control. We conclude that each model captures relevant aspects of the mechanisms underlying attentional control, which we here incorporate into one overarching functional-anatomical model of spatial attention control.
