A head direction cell model based on a spiking neural network with landmark-free calibration_Journal of Biomedical Engineering

Authors：

 YU Naigong ^1,2 , HUANG Jingsen ^1,2 , LIN Ke ^1,2 , ZHANG Zhiwen ^1,2

1. School of Information Science and Technology, Beijing University of Technology, Beijing 100124, P. R. China;
2. Beijing Key Laboratory of Computational Intelligence and Intelligent Systems, Beijing 100124, P. R. China;

Corresponding author：

YU Naigong, Email: yunaigong@bjut.edu.cn

Keywords：

[Key words] Head direction cells; Entorhinal—hippocampus; Error correction; Localization

DOI：

10.7507/1001-5515.202503025

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

In animal navigation, head direction is encoded by head direction cells within the olfactory–hippocampal structures of the brain. Even in darkness or unfamiliar environments, animals can estimate their head direction by integrating self-motion cues, though this process accumulates errors over time and undermines navigational accuracy. Traditional strategies rely on visual input to correct head direction, but visual scenes combined with self-motion information offer only partially accurate estimates. This study proposed an innovative calibration mechanism that dynamically adjusts the association between visual scenes and head direction based on the historical firing rates of head direction cells, without relying on specific landmarks. It also introduced a method to fine-tune error correction by modulating the strength of self-motion input to control the movement speed of the head direction cell activity bump. Experimental results showed that this approach effectively reduced the accumulation of self-motion-related errors and significantly enhanced the accuracy and robustness of the navigation system. These findings offer a new perspective for biologically inspired robotic navigation systems and underscore the potential of neural mechanisms in enabling efficient and reliable autonomous navigation.

1.	Westeinde E A, Kellogg E, Dawson P M, et al. Transforming a head direction signal into a goal-oriented steering command. Nature, 2024, 626(8000): 819-826.
2.	廖诣深, 于乃功. 基于大鼠大脑内嗅-海马-前额叶信息传导回路的空间导航方法. 生物医学工程学杂志, 2024, 41(1): 80-89.
3.	Ji Z, Lomi E, Jeffery K, et al. Phase precession relative to turning angle in theta-modulated head direction cells. Hippocampus, 2025, 35(2): e70008.
4.	刘晨, 熊智, 华冰, 等. 基于位置细胞与网格细胞信息融合的类脑导航方法. 中国空间科学技术(中英文), 2025, 45(1): 113-123.
5.	Taube J S, Muller R U, Ranck J B. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci, 1990, 10(2): 420-435.
6.	Taube J S. The discovery of head direction cells: A personal account. Hippocampus, 2024, 35(1): e23670.
7.	Long X Y, Wang X X, Deng B, et al. Intrinsic bipolar head-direction cells in the medial entorhinal cortex. Adv Sci, 2024, 11(40): e2401216.
8.	陈胤, 隋建峰. 头朝向细胞研究进展. 中华神经医学杂志, 2005(10): 101-103.
9.	Hulse B K, Jayaraman V. Mechanisms underlying the neural computation of head direction. Annu Rev Neurosci, 2020, 43(1): 31-54.
10.	Blanco-Hernández E, Balsamo G, Preston-Ferrer P, et al. Sensory and behavioral modulation of thalamic head-direction cells. Nat Neurosci, 2024, 27(1): 28-33.
11.	Taube J S, Butler W N, Dumont J R, et al. Generating the head direction signal: Two types of head direction cells in the lateral mammillary nuclei and dorsal tegmental nuclei. bioRxiv, 2025: 2025.04.11.648409.
12.	Stratton P, Milford M, Wyeth G, et al. Using strategic movement to calibrate a neural compass: A spiking network for tracking head direction in rats and robots. PLoS ONE, 2011, 6(10): e25687.
13.	Tang Z H, Wang X P, Yang C, et al. A bionic localization memristive circuit based on spatial cognitive mechanisms of hippocampus and entorhinal cortex. IEEE Trans Biomed Circuits Syst, 2024, 18(3): 552-563.
14.	Bicanski A, Burgess N. Environmental anchoring of head direction in a computational model of retrosplenial cortex. J Neurosci, 2016, 36(46): 11601-11618.
15.	Grieves R M, Shinder M E, Rosow L K, et al. The neural correlates of spatial disorientation in head direction cells. eNeuro, 2022, 9(6): ENEURO.0174-22.2022.
16.	Sharp P E, Tinkelman A, Cho J. Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: Implications for path integration in the head direction cell circuit. Behav Neurosci, 2001, 115(3): 571-588.
17.	Song P C, Wang X J. Angular path integration by moving “hill of activity”: A spiking neuron model without recurrent excitation of the head-direction system. J Neurosci, 2005, 25(4): 1002-1014.
18.	Yan Y J, Burgess N, Bicanski A. A model of head direction and landmark coding in complex environments. PLoS Comput Biol, 2021, 17(9): e1009434.
19.	Goodridge J P, Touretzky D S. Modeling attractor deformation in the rodent head-direction system. J Neurophysiol, 2000, 83(6): 3402-3410.
20.	Redish A D, Elga A N, Touretzky D S. A coupled attractor model of the rodent head direction system. Netw Comput Neural Syst, 1996, 7(4): 671-685.
21.	Skaggs W E, Knierim J J, Kudrimoti H S, et al. A model of the neural basis of the rat's sense of direction// Touretzky D S, Tesauro G, Leen T K, et al. Advances in neural information processing systems. Cambridge: MIT Press, 1995, 7: 173-180.
22.	Stentiford R, Knowles T C, Pearson M J. A spiking neural network model of rodent head direction calibrated with landmark free learning. Front Neurorobot, 2022, 16: 867019.
23.	Bing Z S, Nitschke D, Zhuang G H, et al. Towards cognitive navigation: A biologically inspired calibration mechanism for the head direction cell network. J Autom Intell, 2023, 2(1): 31-41.
24.	Nitzan N, Buzsáki G. Physiological characteristics of neurons in the mammillary bodies align with topographical organization of subicular inputs. Cell Rep, 2024, 44(7): 114539.
25.	Street J S, Jeffery K J. The dorsal thalamic lateral geniculate nucleus is required for visual control of head direction cell firing direction in rats. J Physiol, 2024, 602(20): 5247-5267.
26.	Sun H, Cai R L, Li R, et al. Conjunctive processing of spatial border and locomotion in retrosplenial cortex during spatial navigation. J Physiol, 2024, 602(19): 5017-5038.
27.	Huang Y, Lin X, Ren H, et al. CLIF: Complementary leaky integrate-and-fire neuron for spiking neural networks// International Conference on Machine Learning. Vienna: PMLR, 2024: 19949-19972.
28.	Eppler J M. PyNEST: A convenient interface to the NEST simulator. Front Neuroinform, 2008, 2: 12.
29.	Knowles T C, Stentiford R, Pearson M J. WhiskEye: A biomimetic model of multisensory spatial memory based on sensory reconstruction// Lepora N, Mura A, Mastrogiovanni F, et al. Towards autonomous robotic systems. Cham: Springer, 2021: 408-418.

1. Westeinde E A, Kellogg E, Dawson P M, et al. Transforming a head direction signal into a goal-oriented steering command. Nature, 2024, 626(8000): 819-826.
2. 廖诣深, 于乃功. 基于大鼠大脑内嗅-海马-前额叶信息传导回路的空间导航方法. 生物医学工程学杂志, 2024, 41(1): 80-89.
3. Ji Z, Lomi E, Jeffery K, et al. Phase precession relative to turning angle in theta-modulated head direction cells. Hippocampus, 2025, 35(2): e70008.
4. 刘晨, 熊智, 华冰, 等. 基于位置细胞与网格细胞信息融合的类脑导航方法. 中国空间科学技术(中英文), 2025, 45(1): 113-123.
5. Taube J S, Muller R U, Ranck J B. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J Neurosci, 1990, 10(2): 420-435.
6. Taube J S. The discovery of head direction cells: A personal account. Hippocampus, 2024, 35(1): e23670.
7. Long X Y, Wang X X, Deng B, et al. Intrinsic bipolar head-direction cells in the medial entorhinal cortex. Adv Sci, 2024, 11(40): e2401216.
8. 陈胤, 隋建峰. 头朝向细胞研究进展. 中华神经医学杂志, 2005(10): 101-103.
9. Hulse B K, Jayaraman V. Mechanisms underlying the neural computation of head direction. Annu Rev Neurosci, 2020, 43(1): 31-54.
10. Blanco-Hernández E, Balsamo G, Preston-Ferrer P, et al. Sensory and behavioral modulation of thalamic head-direction cells. Nat Neurosci, 2024, 27(1): 28-33.
11. Taube J S, Butler W N, Dumont J R, et al. Generating the head direction signal: Two types of head direction cells in the lateral mammillary nuclei and dorsal tegmental nuclei. bioRxiv, 2025: 2025.04.11.648409.
12. Stratton P, Milford M, Wyeth G, et al. Using strategic movement to calibrate a neural compass: A spiking network for tracking head direction in rats and robots. PLoS ONE, 2011, 6(10): e25687.
13. Tang Z H, Wang X P, Yang C, et al. A bionic localization memristive circuit based on spatial cognitive mechanisms of hippocampus and entorhinal cortex. IEEE Trans Biomed Circuits Syst, 2024, 18(3): 552-563.
14. Bicanski A, Burgess N. Environmental anchoring of head direction in a computational model of retrosplenial cortex. J Neurosci, 2016, 36(46): 11601-11618.
15. Grieves R M, Shinder M E, Rosow L K, et al. The neural correlates of spatial disorientation in head direction cells. eNeuro, 2022, 9(6): ENEURO.0174-22.2022.
16. Sharp P E, Tinkelman A, Cho J. Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of Gudden in the rat: Implications for path integration in the head direction cell circuit. Behav Neurosci, 2001, 115(3): 571-588.
17. Song P C, Wang X J. Angular path integration by moving “hill of activity”: A spiking neuron model without recurrent excitation of the head-direction system. J Neurosci, 2005, 25(4): 1002-1014.
18. Yan Y J, Burgess N, Bicanski A. A model of head direction and landmark coding in complex environments. PLoS Comput Biol, 2021, 17(9): e1009434.
19. Goodridge J P, Touretzky D S. Modeling attractor deformation in the rodent head-direction system. J Neurophysiol, 2000, 83(6): 3402-3410.
20. Redish A D, Elga A N, Touretzky D S. A coupled attractor model of the rodent head direction system. Netw Comput Neural Syst, 1996, 7(4): 671-685.
21. Skaggs W E, Knierim J J, Kudrimoti H S, et al. A model of the neural basis of the rat's sense of direction// Touretzky D S, Tesauro G, Leen T K, et al. Advances in neural information processing systems. Cambridge: MIT Press, 1995, 7: 173-180.
22. Stentiford R, Knowles T C, Pearson M J. A spiking neural network model of rodent head direction calibrated with landmark free learning. Front Neurorobot, 2022, 16: 867019.
23. Bing Z S, Nitschke D, Zhuang G H, et al. Towards cognitive navigation: A biologically inspired calibration mechanism for the head direction cell network. J Autom Intell, 2023, 2(1): 31-41.
24. Nitzan N, Buzsáki G. Physiological characteristics of neurons in the mammillary bodies align with topographical organization of subicular inputs. Cell Rep, 2024, 44(7): 114539.
25. Street J S, Jeffery K J. The dorsal thalamic lateral geniculate nucleus is required for visual control of head direction cell firing direction in rats. J Physiol, 2024, 602(20): 5247-5267.
26. Sun H, Cai R L, Li R, et al. Conjunctive processing of spatial border and locomotion in retrosplenial cortex during spatial navigation. J Physiol, 2024, 602(19): 5017-5038.
27. Huang Y, Lin X, Ren H, et al. CLIF: Complementary leaky integrate-and-fire neuron for spiking neural networks// International Conference on Machine Learning. Vienna: PMLR, 2024: 19949-19972.
28. Eppler J M. PyNEST: A convenient interface to the NEST simulator. Front Neuroinform, 2008, 2: 12.
29. Knowles T C, Stentiford R, Pearson M J. WhiskEye: A biomimetic model of multisensory spatial memory based on sensory reconstruction// Lepora N, Mura A, Mastrogiovanni F, et al. Towards autonomous robotic systems. Cham: Springer, 2021: 408-418.

Journal of Biomedical Engineering

Latest ArticlesA head direction cell model based on a spiking neural network with landmark-free calibration

Abstract Full text Figures/Tables Video References Cited by

Format

Content