Listening to numbers affects visual and haptic bisection in healthy individuals and neglect patients
Highlights
► Numbers are represented in a spatial format, the mental number line (MNL). ► The MNL has been found to affect space representation. ► Here we show that listening to numbers affects visual and haptic line bisection. ► Critically, this effect was observed also in patients with left unilateral neglect. ► Neglect does not prevent a crossmodal interaction between numbers and space.
Introduction
Numbers are typically represented in a spatial format that takes the form of a mental number line (MNL; see Dehaene, Bossini, & Giraux, 1993), that – in left-to-right reading cultures – appears to be left-to-right oriented. Accordingly, small numbers occupy the left side of the MNL, and large numbers the right side. There is evidence for similar biases in the way attention is allocated to physical space, and to the space of the MNL. In particular, neurologically unimpaired individuals tend to show a leftward directional bias – often referred to as “pseudoneglect” (for a review, see Jewell & McCourt, 2000) – both when bisecting physical lines and numerical intervals (Cattaneo et al., 2010, Longo and Lourenco, 2007), although the mechanisms underlying pseudoneglect for numerical and physical lines bisection may not overlap completely (e.g., Ashkenazi & Henik, 2010).
Importantly, the spatial representation of numbers and the perception of physical space affect each other (see Umiltà et al., 2009, Wood et al., 2008, for reviews). For instance, visually presented small numbers bias attention toward the left side of physical space, and visually presented large numbers bias attention to the right side of it (Fischer, Castel, Dodd, & Pratt, 2003). Correspondingly, activating the representation of specific portions of space affects numerical processing (Cattaneo et al., 2011a, Stoianov et al., 2008). Such interaction can also occur across sensory modalities: in particular, listening to small and large magnitude numbers while haptically estimating the length of a rod shifts its perceived midline respectively to the left and to the right of the true midpoint in neurologically unimpaired participants (Cattaneo et al., 2010).
Critically, whether space perception is affected by processing numerical magnitudes to a similar extent in different sensory modalities is not known so far. A recent study demonstrates that auditorily presented numbers affect length estimation of haptically perceived rods (Cattaneo et al., 2010), but whether this effect is also present and – if so – to a similar extent when the length of visually presented rods has to be judged has not been investigated yet. In fact, it could prove to be the case that the visual modality is more “resistant” against the attentional biases induced by the concurrent auditory presentation of numbers, being vision usually the most precise modality for judging spatial location and spatial extent (with the modality that “dominates” in a specific situation being the one that is more precise for the task being performed, see Ernst and Banks, 2002, Welch and Warren, 1986).
Moreover, it has not been previously investigated whether auditorily presented numbers can affect the representation of space in patients affected by unilateral spatial neglect (USN). This is a deficit, typically brought about by right hemispheric lesions, whereby patients are not able to report stimuli presented in the portion of space contralateral to the side of the lesions (namely, the left-hand-side in right-brain-damaged patients), and to explore that side of space (Halligan et al., 2003, Heilman et al., 2003, Husain, 2008, Vallar, 1998, Vallar, 2001). One task frequently used to assess USN – both for diagnostic and research purposes – is “line bisection”, where participants are required to mark the perceived mid-point of a line that, in order to assess lateral USN, is presented horizontally. Right-brain-damaged patients with left USN typically bisect the line to the right of the veridical midpoint, therefore underestimating its left portion (Bisiach et al., 1983a, Bisiach et al., 1976, Schenkenberg et al., 1980, Vallar et al., 2000). Notably, also the horizontal spatial representation of numbers is distorted in USN patients (despite a spared abstract knowledge of numerical quantities, see Pia et al., 2009, Vuilleumier et al., 2004). In particular, right-brain-damaged patients with left USN may show a rightward bias in setting the mid-point of auditorily presented numerical intervals (Zamarian et al., 2007, Zorzi et al., 2002), and a representational neglect of the left portion of the MNL in other paradigms such as judging whether a given number represents the midpoint of a numerical interval (Hoeckner et al., 2008), or comparing numerical magnitudes (Vuilleumier et al., 2004). Interestingly, in a left-brain-damaged patient with right USN, an opposite pattern has been described (Pia et al., 2009).
Other interactions between spatial and numerical representations, however, appear not to be prevented by USN: in particular, numbers presented visually at the extremities of a to-be-bisected visual line affect the bisection performance of right-brain-damaged patients with left USN (Bonato, Priftis, Marenzi, & Zorzi, 2008). Specifically, the bisection error is displaced leftward (i.e., contralaterally with respect to the side of the lesion) when a small digit is presented, and rightward (i.e., ipsilaterally to the side of the lesion) when a large digit is presented (for reviews on the relationship between spatial and numerical representations see de Hevia et al., 2008, Umiltà et al., 2009). So far, no studies have ever investigated whether listening to task-irrelevant numbers affects spatial judgments in the visual and haptic modality in right-brain-damaged patients with USN, as assessed by line bisection. In this study, a group of neurologically unimpaired participants and a group of patients with right hemisphere lesions, with and without evidence of left USN, were required to bisect rods of different length in the visual and haptic modalities, while concurrently listening to numerical cues of a different magnitude. Were the attentional modulation induced by numbers processing the same across sensory modalities, putative shifts in the bisection bias should be comparable in the visual and in the haptic tasks. Moreover, finding evidence for an effective modulation by auditorily presented numbers on bisection performance in right-brain-damaged patients with left USN shall contribute to shed light on the nature of the attentional deficits induced by USN, and on the neural circuits mediating numbers-space interactions in neurologically unimpaired individuals.
Section snippets
Participants
Nineteen patients with right hemisphere brain lesions, confirmed by CT or MRI scan, participated in the study and were recruited from the inpatient population of the Neurorehabilitation Unit of the IRCCS Italian Auxological Institute, Milan, and of the Neuropsychological Unit, Ospedali Civili di Brescia, Brescia, Italy. Patients gave written informed consent to the study, that was approved by the Ethical Committee of the IRCCS Italian Auxological Institute, Milan, Italy. The patients’
Baseline (i.e., silent) condition
Fig. 2 shows the mean LBE for the N+, N−, and the two control groups in the baseline visual and haptic bisection conditions. Unimpaired participants overall showed a leftward bisection bias both in the visual and in the haptic modality. A similar pattern was observed in the N− patients, also erring to the left in both modalities. Conversely, the N+ group showed a rightward bias in the visual modality and a leftward bias in the haptic modality.
A repeated-measures analysis of variance (ANOVA) on
Discussion
In this study, patients with right hemisphere damage (with and without USN) and neurologically unimpaired individuals are required to estimate the midpoint of a series of rods either visually or haptically explored while listening, in certain conditions, to either a number of different magnitude (“2” and “8”), or to a neutral syllable (“blah”). Performing the task while listening to task-irrelevant numbers affects performance in all participants. In particular, listening to a small digit (“2”)
Acknowledgments
GV has been supported by a FAR Grant 2011 from the University of Milano-Bicocca, and by a Ricerca Corrente Grant from the Italian Auxological Institute, Milan, Italy. We are grateful to Marcello Gallucci and Marco Perugini for their statistical advice and to the patients that took part in the study for their forbearance.
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