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Effects of Strategies on Mental Rotation and Hemispheric Lateralization: Neuropsychological Evidence

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Effects of Strategies on Mental Rotation and Hemispheric Lateralization: Neuropsychological Evidence Effects of Strategies on Mental Rotation and Hemispheric Lateralization: Neuropsychological Evidence Barbara Tomasino and Raffaella I. Rumiati Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/5/878/1758193/089892904970753.pdf by guest on 18 May 2021 Abstract & We can predict how an object would look if we were to view that what matters is the type of strategy adopted in MR. see it from different viewpoints by imagining its rotation. This Thus, independently of the type of stimulus, patients with left essential human ability, called mental rotation (MR), guides hemisphere lesions showed a selective deficit in MR as a individuals’ actions by constantly updating their environmental consequence of their manual activity, whereas patients with consequences. It is, however, still under debate whether the right hemisphere lesions were found impaired in MR by means way in which our brain accomplishes this operation is deter- of a visual strategy. We conclude that MR is achieved by mined by the type of stimulus or rather by a mental strategy. recruiting different strategies, implicitly triggered or prompted Here we present neuropsychological evidence sustaining the at will, each sustained by a unilateral brain network. & INTRODUCTION selectively impaired when deciding whether a hand is Typically, mental rotation (MR) is studied by asking left or right despite being still able to mentally rotate subjects to decide whether two images—of which one Shepard and Metzler’s stimuli (Rumiati et al., 2001). On is either a mirror or an identical rotated image of the the other hand, a patient (JB) with a bilateral infero- other—are the same or different (Corballis, 1997; She- temporal lesion was reported as having a deficit in per- pard & Metzler, 1971; Shepard & Cooper, 1982). The forming MR of Shepard and Metzler’s stimuli (Sirigu analysis of the response times (RTs) shows that subjects & Duhamel, 2001). However, JB’s ability to mentally create an internal image of an object and that they rotate rotate motor images of body parts was not investigated. it until it is congruent with the target object. A linear Nor was this ability assessed in other posterior left increase in RTs with increasing angular disparity is usu- (Morton & Morris, 1995; Metha & Newcombe, 1991; ally found for rotated stimuli such as two-dimensional Kosslyn, Holtzman, Farah, & Gazzaniga, 1985) or right alphanumeric characters (Corballis & Sergent, 1989) and (Bricolo, Shallice, Priftis, & Meneghello, 2000; Ditunno three-dimensional Shepard and Metzler’s stimuli (Cohen & Mann, 1990; Farah & Hammond, 1988; Ratcliff, 1979) et al., 1996; Shepard & Metzler, 1971; Shepard & Coo- brain-damaged patients who have also been described per, 1982). MR operations can be distinguished accord- as having a deficit of MR operations. In a recent study ing to the type of stimulus involved (Tomasino, Toraldo, (Tomasino et al., 2003), a direct comparison between & Rumiati, 2003; Rumiati, Tomasino, Vorano, Umilta`,& right hemisphere (RH) and left hemisphere (LH) pa- DeLuca, 2001; Kosslyn, DiGirolamo, Thompson, & Al- tients’ performance on MR of both types of stimuli pert, 1998), the reference frame (Zacks, Rypma, Gabrieli, showed that lesions in the LH impaired MR of hands, Tversky, & Glover, 1999; Zacks, Mires, Tversky, & Ha- while lesions in the RH affected MR of external objects zeltine, 2000; Zacks, Ollinger, Sheridan, & Tversky, 2002; (e.g., a puppet and flag shapes). Wraga, Creem, & Proffitt, 1999), or the strategies used Psychophysical studies indicate that different mecha- (Kosslyn, Thompson, Wraga, & Alpert, 2001). nisms may be selected in MR according to the frame As far as the stimulus type is concerned, different of reference used for the rotation (Zacks et al., 2000). operations may be recruited in MR depending on Thus, MR can be accomplished taking as a reference whether the stimulus type is a body part or a two- frame the object itself (i.e., allocentric view) or the or three-dimensional object. Neuropsychological studies viewer’s (i.e., egocentric view). It has been shown that indicate that these two types of transformations can be the allocentric and egocentric transformations lead to selectively affected. For instance, a patient with left different chronometric patterns. A strong correlation hemisphere (LH) brain damage was described as being between the angle of rotation and RTs has been consist- ently obtained in subjects who mentally rotated the stimuli using the allocentric view (Zacks et al., 1999, Scuola Internazionale Superiore di Studi Avanzati (SISSA) 2000, 2002; Wraga et al., 1999; Corballis, 1997; Shepard D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:5, pp. 878–888 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/089892904970753 by guest on 27 September 2021 & Metzler, 1971; Shepard & Cooper 1982). When trans- The present study was designed first to provide formations are based on the viewer’s perspective, the neuropsychological evidence that object- and viewer- RTs reflect biomechanical constraints that mirror those based transformations are dissociable as an effect of of the real movements (Zacks et al., 2000; Parsons, brain damage. We assumed that any lesion of the brain 1987a, 1987b, 1994). network (i.e., parietal or premotor cortex) that is known Functional imaging studies have investigated how MR to underlie MR abilities will selectively impair object- or can be modulated as an effect of the type of stimuli, the egocentric-based transformation as a consequence of type of strategies, and reference frames. In a PET study damage to the RH or to the LH, respectively. We (Kosslyn et al., 1998) with healthy participants, it was also aimed to reconcile the neuropsychological findings, shown that MR of hands enhanced activation in the left calling for a hemispheric specialization in stimulus- de- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/5/878/1758193/089892904970753.pdf by guest on 18 May 2021 parietal lobe, left motor and premotor areas, whereas MR pendent MR (Tomasino et al., 2003), with the recently of Shepard and Metzler’s stimuli induced a bilateral proposed ‘‘strategy account’’ (Kosslyn et al., 2001). activation of the parietal lobe and BA 19 only. Based on We addressed these issues by asking patients with these activations, Kosslyn et al. (1998) argued that MR of unilateral brain lesions and healthy control subjects the hands but not of Shepard and Metzler’s stimuli were instructed to adopt a motor (egocentric transfor- recruits motor processes. Interestingly, the same activa- mation) and, in a different block, a visual strategy (allo- tion patterns were obtained in another PET study (Koss- centric transformation) when performing MR of hand lyn et al., 2001) in which subjects performed MR of shapes (Experiment 1) or Shepard and Metzler’s stimuli Shepard and Metzler’s stimuli using an internal or exter- (Experiment 2). nal strategy. Thus, they imagined rotating a stimulus as Independently of the stimulus to be rotated, patients a consequence of their own hand action (i.e., internal with LH lesions are expected to make considerably strategy) or as if they were observing the stimulus more errors than RH patients in applying the motor rotating in the visual space (i.e., external strategy). The strategy, as it is well known that the LH sustains tasks left primary motor cortex—the region that in Kosslyn’s that require actual and simulated hand movements PET study (Kosslyn et al., 1998) was activated in associ- (Tomasino et al., 2003; Rumiati et al., 2001; Kosslyn ation with MR of hands only—was here enhanced when et al., 1998, 2001; Ganis, Keenan, Kosslyn, & Pascual subjects mentally rotated Shepard and Metzler’s stimuli, Leone, 2000; Parsons & Fox, 1998; Sirigu et al., 1996; simulating a sort of manual rotation. The effect of the Decety et al., 1994). In sharp contrast, given that the RH reference frame on MR was investigated in a series of is held to be involved in spatial operations (Kosslyn studies (Zacks et al., 1999, 2002). First, it was shown that et al., 2001; Bricolo et al., 2000; Harris et al., 2000; when subjects decided which arm of a puppet was out- Davidoff & Warrington, 1999; Zacks et al., 1999; Corbal- stretched, the activation within the PTO junction was lis, 1997; Ditunno & Mann, 1990; Farah & Hammond, lateralized to the LH when the stimuli were upright 1988; Ratcliff, 1979), we predict that RH patients should (egocentric perspective MR), whereas it was stronger be less accurate than the LH patients in performing the in the RH for upside-down pictures (object-based MR) MR using the visual strategy. To date, we refer to LH/ (Zacks et al., 1999). These results were partially repli- RH as patients with lesions in any region of the brain cated in a successive fMRI study (Zacks et al., 2002), network (i.e., parieto-premotor) sustaining MR in the where subjects were presented with disoriented pairs of LH and RH, respectively. human shapes depicted with an extended arm. The activation was lateralized to the RH posterior cortex when subjects performed same–different judgments RESULTS (object-based MR) compared with when they made left–right judgments on which arm was extended (viewer- Independent of the type of stimulus (i.e., hand shapes or based MR). However, the opposite comparison (i.e., Shepard and Metzler’s stimuli), a double dissociation was viewer-based transformation vs. object-based transfor- found between deficits of motor and visual strategies in mation) did not show any lateralized activity. performing MR. Thus, RH patients (RHD1 and RHD2) Zacks et al. (1999, 2002) proposed a model that pre- were more accurate than LH patients (LHD1 and LHD2) dicts the presence of a double dissociation between when they imagined physically turning the stimulus. regions specifically associated with MR obtained by On the contrary, LH patients (LHD1 and LHD2) were adapting the egocentric reference frame of the viewer better than RH patients (RHD1 and RHD2) when they to that of the object, and those associated with MR imagined the stimulus as rotating in the visual space.
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