How number processing survives left occipito-temporal damage

Abstract

We investigated the neural systems that support number processing in a patient (JL) who had damage to the left ventral occipito-temporal cortex (LvOT). JL had severely impaired written word recognition but he was remarkably accurate in number tasks, albeit slower than normal. This suggests LvOT activation is necessary for efficient but not for accurate number decisions. Here we investigated how JL made accurate number decisions using fMRI; we compared JL's brain activation to that in healthy controls and in two patients with frontal lobe damage who, like JL, made slow but accurate responses in number tasks. For semantic relative to perceptual decisions on numbers, JL did not activate the left occipito-temporal area that was involved in all other subjects. However, JL had significantly increased activation in a left posterior middle temporal region. In addition, during semantic and perceptual decisions on numbers, JL showed increased activation in: (1) the right occipito-temporal cortex, (2) right caudate, and (3) bilateral frontal regions. These effects were unique to JL and cannot be explained in terms of abnormally long response times because they were not observed in the other patients who made slow but accurate number decisions. Together these results show that although the LvOT usually contributes to efficient number processing, activation in this region is not essential for accurate performance because (i) perceptual processing of numbers can be supported by right occipital, right caudate, and bilateral frontal activation and (ii) semantic processing of numbers can be supported by increased left posterior middle temporal activation associated with hand actions.

Figure 1.

LvOT activation for numbers in healthy controls at the site of the lesion in JL. Controls’ activations in LvOT regions on (A) a rendered brain, (B) sections, and (C) sections showing JL's lesion.

Figure 3.

Experimental design. The same semantic (quantity and category tasks) and perceptual color decision tasks were used with pairs of Arabic numbers (left panel) and object names (right panel) which were presented in one of four possible colors (red, yellow, blue, green). In each trial, participants viewed pairs of stimuli presented one above the other with a fixation cross in the middle of the computer screen. Subjects were instructed to indicate with a button press which of the two stimuli was the correct response to a question consisting of two keywords presented above the upper stimulus before and during the stimulus display. For each task, one of two possible questions was presented in different blocks in counterbalanced order (i.e., quantity: ‘larger/smaller’ and ‘more/less’; category: ‘summer/winter’ and ‘working/sleeping’ for the semantic tasks; ‘red/yellow/blue/green item?’ for the color-decision task, see Cappelletti et al., 2010 for more details). [To view this figure in color, please visit the online version of this Journal.]

Figure 2.

Patients B and T brain lesions.

Figure 4.

JL's activation in number tasks. JL's activations (top panel) and over-activations (bottom panel) during the number tasks on a rendered brain (left side) and on axial sections (right side) of JL's brain.

Figure 5.

Activation in JL above all other participants. Plot of the parameter estimates in left middle temporal regions (MTG, top panel) and right caudate (bottom panel) showing stronger activation during number tasks in JL (black bars) relative to patients B and T with similar response times and to all controls (C; age-matched in filled circles).

Figure 6.

Atypical activation patterns in JL relative to patients B and T and to controls. Using the fuzzy clustering algorithm (Seghier, Friston & Price, 2007), atypical activation patterns are identified by assessing the contribution of each subject to response profiles in voxels that survive a classical F-statistic criterion. The output identifies subjects, like JL, who drive activation in voxels distributed across the whole neural system rather than at the voxel level. This showed that abnormally high activation in JL during the number tasks, indicated by the horizontal line, was not an inevitable consequence of a single subject comparison to a normal group.