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Distinct neuronal representation of small and large numbers in the human medial temporal lobe

Abstract

Whether small numerical quantities are represented by a special subitizing system that is distinct from a large-number estimation system has been debated for over a century. Here we show that two separate neural mechanisms underlie the representation of small and large numbers. We performed single neuron recordings in the medial temporal lobe of neurosurgical patients judging numbers. We found a boundary in neuronal coding around number 4 that correlates with the behavioural transition from subitizing to estimation. In the subitizing range, neurons showed superior tuning selectivity accompanied by suppression effects suggestive of surround inhibition as a selectivity-increasing mechanism. In contrast, tuning selectivity decreased with increasing numbers beyond 4, characterizing a ratio-dependent number estimation system. The two systems with the coding boundary separating them were also indicated using decoding and clustering analyses. The identified small-number subitizing system could be linked to attention and working memory that show comparable capacity limitations.

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Fig. 1: Behavioural task, stimuli and behavioural performance.
Fig. 2: Responses of number-selective neurons.
Fig. 3: Tuning characteristics of number-selective neurons.
Fig. 4: SVM classification analysis.
Fig. 5: Population state-space analysis and k-means clustering.

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Data availability

The data associated with this study are publicly available at https://github.com/EstherKutter/Distinct-Neuronal-Representation-Of-Small-And-Large-Numbers-In-The-Human-MTL.

Code availability

The custom code associated with this study is publicly available at https://github.com/EstherKutter/Distinct-Neuronal-Representation-Of-Small-And-Large-Numbers-In-The-Human-MTL.

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Acknowledgements

We thank all patients for their participation. This research was supported by the German Research Council (Mo 930/4-2, SPP 2205, SPP 2411, SFB 1089; Ni 618/11-1, SPP 2205), the BMBF (031L0197B) and a NRW Network Grant (iBehave). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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A.N. and F.M. designed the study; R.S. and F.M. recruited patients; V.B. and F.M. implanted the electrodes; E.F.K. and G.D. collected the data; E.F.K. and A.N. analysed the data with contributions from F.M.; A.N., E.F.K. and F.M. wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Florian Mormann or Andreas Nieder.

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Kutter, E.F., Dehnen, G., Borger, V. et al. Distinct neuronal representation of small and large numbers in the human medial temporal lobe. Nat Hum Behav 7, 1998–2007 (2023). https://doi.org/10.1038/s41562-023-01709-3

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