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Common neural substrates for ordinal numerical representations and ordinal representations in short-term memory

Lucie Attout1*, Wim Fias2 and Steve Majerus1
  • 1 University of Liège, Department of Cognitive Sciences, Belgium
  • 2 Ghent University, Department of Experimental Psychology, Belgium

Introduction
The retention of order information, that is, the serial order in which events have occurred, is a critical dimension of short-term memory (STM). However, although many models of order STM have been developed, the exact nature of representations used to code order information in STM tasks remains unknown. The current study explores the hypothesis that the neural substrates allowing for coding of ordinal information in the numerical domain also support the coding of order information in STM. This hypothesis is supported by several recent findings. First, several neuroimaging studies have shown that a specific region in the parietal cortex, the anterior intraparietal sulcus (IPS), is active both during coding of order information in STM tasks (Majerus et al., 2006, 2010) as well as during ordinal judgment of numerical information (Kaufmann et al., 2009). Second, at a behavioral level, the SNARC effect, a hallmark effect of ordinal numerical processing, has also been observed in STM tasks: van Dijck and Fias showed that a right-hand response to items held in STM is faster than a left-hand response to items stemming from late positions, and vice-versa for items from early positions, mirroring the SNARC effect observed in numerical judgment tasks (van Dijck and Fias, 2011). In addition, Marshuetz et al. (2006) showed that the distance effect typically observed in number comparison tasks can also appear in order STM tasks, where participants take more time to judge items from close versus distant serial positions. These studies provide evidence for overlapping processes supporting ordinal representations in the numerical and the STM domains. However, as so far, no neuroimaging study has directly compared the neural substrates involved in ordinal processing during number and STM tasks.

Objectives
We designed an fMRI experiment that directly compared ordinal processing in numerical and STM tasks, by comparing the neural substrates of ordinal distance effects in numerical judgment and order STM tasks. Using a parametric design, we tested whether the anterior IPS, shown to be active during both STM and ordinal number judgment tasks, is sensitive to ordinal distance effects in both STM and numerical domains.

Methods
The neural substrates of ordinal processing in STM were assessed using a delayed order probe recognition task. For a given list of letters to be maintained (e.g., ‘D, C, I, F, J, A’), the participants had to judge, after a variable retention delay (mean: 6 seconds), whether a target letter had occurred before another target letter in the memory list (e.g., ‘C’ ‘F’ ?). The positional distance between the two target letters varied from 2 to 5, while keeping the alphabetical distance constant. The neural substrates of ordinal processing for number information was assessed using a numerical judgment task where the participant had to decide whether a numerical stimulus (e.g., ‘45’), occurs before a numerical standard (e.g., ‘65’) or not (Pinel et al., 2001); distances to be assessed ranged from 1-7 units. Finally, a luminance judgment condition was administered, where two letters were presented with identical or differing luminance levels; luminance differences between the two letters varied, allowing to assess a luminance distance effect similar to the numerical and STM distance effects. The luminance condition had been designed to control for any distance-related brain activations not due to ordinal processing, such as mere differences in trial difficulty and related cognitive effort. The participants were 25 healthy young adults (mean age: 20.5 ± 2 years). In all tasks, distance effects were assessed using parametric modulation regression designs.

Results
First, we observed that the numerical distance effect in the numerical judgment task activated both the left and the right anterior IPS, reproducing earlier findings (Fias et al., 2007; Pinel et al., 2001). Second, we also observed significant modulation of brain activation by the distance of positions to be judged in the STM task. The STM distance effect involved both the left and right IPS. Null conjunction analysis over the distance effects in both STM and numerical processing tasks confirmed that the IPS regions supporting the distance effects were indeed overlapping in both conditions. This overlap of neural activation in IPS areas was not driven by mere differences in task difficulty of the distances to be judged, since the distance effects in IPS regions for the STM and numerical tasks remained significant after controlling for any IPS activity related to non-ordinal distance judgment in the luminance control condition. Finally, a specific analysis of the different phases of the STM task showed that the IPS regions responding to distance effects during order STM retrieval and numerical judgment were also active during STM maintenance, suggesting that distance-sensitive IPS areas are also those that support STM maintenance of order information.

Discussion
These findings constitute a first direct demonstration of shared neural correlates for processing of order information in the STM and number domains, via the assessment of neural substrates associated with ordinal distance effects in both domains. These results rise the intriguing idea that the bilateral anterior IPS host a common representational system for order information in STM and numerical cognition. The common activations in the bilateral IPS observed here cannot be simply ascribed to a greater attentional involvement for difficult (close position) trials, since we controlled for this possibility via the luminance judgment condition. Some studies proposed that order is coded in an abstract ordinal format and that these codes could serve order representation in several cognitive domains (Walsh, 2003; Marshuetz et al., 2006; Fias et al., 2007). More precisely, neural network models have implemented order coding in STM as stemming from the application of ordinal ranks shared with numerical cognition and have pinpointed to the role of the IPS in creating these ordinal codes, without providing any direct evidence (Botvinick and Watanabe, 2007). The present study provides the first compelling evidence for a neuroanatomical overlap of ordinal coding in STM and numerical domains, and open new perspectives for the understanding of interactions between STM and numerical cognition.

References

Botvinick, M., and Watanabe, T. (2007). From numerosity to ordinal rank: a gain-field model of serial order representation in cortical working memory. Journal of Neuroscience 27, 8636-8642.
Fias, W., Lammertyn, J., Caessens, B., and Orban, G.A. (2007). Processing of abstract ordinal knowledge in the horizontal segment of the intraparietal sulcus. Journal of Neuroscience 27, 8952-8956.
Kaufmann, L., Vogel, S., Starke, M., Kremser, C., and Schocke, M. (2009). Numerical and non-numerical ordinality processing in children with and without developmental dyscalculia: Evidence from fMRI. Cognitive Development 24, 486-494.
Majerus, S., D'argembeau, A., Martinez Perez, T., Belayachi, S., Van Der Linden, M., Collette, F., Salmon, E., Seurinck, R., Fias, W., and Maquet, P. (2010). The commonality of neural networks for verbal and visual short-term memory. Journal of cognitive neuroscience 22, 2570-2593.
Majerus, S., Poncelet, M., Van Der Linden, M., Albouy, G., Salmon, E., Sterpenich, V., Vandewalle, G., Collette, F., and Maquet, P. (2006). The left intraparietal sulcus and verbal short-term memory: Focus of attention or serial order? Neuroimage 32, 880-891.
Marshuetz, C., Reuter-Lorenz, P., Smith, E., Jonides, J., and Noll, D. (2006). Working memory for order and the parietal cortex: an event-related functional magnetic resonance imaging study. Neuroscience 139, 311-316.
Pinel, P., Dehaene, S., Riviere, D., and Lebihan, D. (2001). Modulation of parietal activation by semantic distance in a number comparison task. Neuroimage 14, 1013-1026.
Van Dijck, J.P., and Fias, W. (2011). A working memory account for spatial-numerical associations. Cognition 114, 114-119.
Walsh, V. (2003). A theory of magnitude: common cortical metrics of time, space and quantity. Trends in Cognitive Sciences 7, 483-488.

Keywords: short term memory, serial order, Numerical cognition, fMRI, distance effect

Conference: Belgian Brain Council, Liège, Belgium, 27 Oct - 27 Oct, 2012.

Presentation Type: Poster Presentation

Topic: Higher Brain Functions in health and disease: cognition and memory

Citation: Attout L, Fias W and Majerus S (2012). Common neural substrates for ordinal numerical representations and ordinal representations in short-term memory. Conference Abstract: Belgian Brain Council. doi: 10.3389/conf.fnhum.2012.210.00047

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Received: 30 Aug 2012; Published Online: 12 Sep 2012.

* Correspondence: Miss. Lucie Attout, University of Liège, Department of Cognitive Sciences, Liège, Belgium, Lucie.attout@ulg.ac.be