Space and time in the brain
Open accessAbstract
Nothing is more intuitive, yet more complex, than the concepts of space and time. In contrast to spacetime in physics, space and time in neuroscience remain separate coordinates to which we attach our observations. Investigators of navigation and memory relate neuronal activity to position, distance, time point, and duration and compare these parameters to units of measuring instruments. Although spatial-temporal sequences of brain activity often correlate with distance and duration measures, these correlations may not correspond to neuronal representations of space or time. Neither instruments nor brains sense space or time. Neuronal activity can be described as a succession of events without resorting to the concepts of space or time. Instead of searching for brain representations of our preconceived ideas, we suggest investigating how brain mechanisms give rise to inferential, model-building explanations.
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Treating space as a sequence is a necessity for humans and other animals because they lack a global positioning system that enables direct sensing of location coordinates.
“Treating space as a sequence is a necessity for humans and other animals because they lack a global positioning system that enables direct sensing of location coordinates.”
From Space is a latent sequence: A theory of the hippocampus (2024) · cites this paper as [9]
In “Representation of space in the brain” (page unavailable), the authors say neurons lack instrument-based distance measurements and that the brain infers trajectories from movement-related cues and neuronal sequences. But “Broader thinking” (page unavailable) presents treating sequential order as space as an approach, not a necessity for all humans and other animals; the paper does not describe a missing global positioning system. (LLM, conf=0.84)
Experimental — accuracy not yet measuredAnomalies have been accumulating over the simple view that place cells represent just locations.
“However, anomalies have been accumulating over the simple view that place cells represent just locations (8, 9, 32, 45, 46).”
From Space is a latent sequence: A theory of the hippocampus (2024) · cites this paper as [9]
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“…by theta oscillations (5–12 Hz) has been proposed to be critical for the self-motion based estimation of linear distance through the integration of speed, distance and time (Burgess, 2008; Buzsaki, 2005; Buzsaki & Llinas, 2017; Hasselmo & Brandon, 2008; Jacob et al., 2017; McNaughton et al., 1996).”
BackgroundSignal processing in the vagus nerve: Hypotheses based on new genetic and anatomical evidence
Shaffer, C., Barrett, L. F., & Quigley, K. S. (2023) · Biological Psychology · doi:10.1016/j.biopsycho.2023.108626 · Cited by 33 · see citing works
The homogenous hippocampus: How hippocampal cells process available and potential goals
McNaughton, N., & Bannerman, D. M. (2024) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2024.102653 · Cited by 32 · see citing works
Space is a latent sequence: A theory of the hippocampus
Raju, R. V., Guntupalli, J. S., Zhou, G., Wendelken, C., Lázaro-Gredilla, M., & George, D. (2024) · Science Advances · doi:10.1126/sciadv.adm8470 · Cited by 25 · see citing works
Buonomano, D. V., Buzsáki, G., Davachi, L., & Nobre, A. C. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1430-23.2023 · Cited by 36 · see citing works
Self-citationBrain representations of space and time in episodic memory: A systematic review and meta-analysis
Torres-Morales, C., & Cansino, S. (2023) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-023-01140-1 · Cited by 29 · see citing works
“In the field of neuroscience, such debates are important, because it remains unknown whether we actually perceive and experience space and time or whether these experiences are created in our brain (Buzsáki & Llinás, 2017).”
BackgroundNiedecker, R. W., Kloc, M. L., Holmes, G. L., & Barry, J. M. (2021) · Epilepsia · doi:10.1111/epi.16927 · Cited by 25 · see citing works
Corticothalamic axon morphologies and network architecture
Rockland, K. S. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13910 · Cited by 26 · see citing works
Mnemonic Content and Hippocampal Patterns Shape Judgments of Time
Sherman, B. E., DuBrow, S., Winawer, J. A., & Davachi, L. (2022) · Psychological Science · doi:10.1177/09567976221129533 · Cited by 25 · see citing works
“Conclusions One theoretical position is that brains, in fact, do not sense time; just because activity in a brain region is correlated with the passage of time does not mean that the region is clocking time per se (Ezzyat & Davachi, 2014; Davachi & DuBrow, 2015; Buzsáki & Llinás, 2017).”
BackgroundNeurophysiology of visually guided eye movements: critical review and alternative viewpoint
Goffart, L., Bourrelly, C., & Quinton, J. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00402.2018 · Cited by 23 · see citing works
“Moreover, as Pellionisz and Llinás (1982) explained, the classical usage of separate space and time coordinates may not be applicable in the case of describing the inner workings of the central nervous system (see also Buzsáki and Llinás 2017).”
BackgroundAAV Delivery of shRNA Against TRPC6 in Mouse Hippocampus Impairs Cognitive Function
Xie, R., Wang, Z., Liu, T., Xiao, R., Lv, K., Wu, C. F., Luo, Y., Cai, Y., & Fan, X. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.688655 · Cited by 18 · see citing works
“The process of separating the components of a complex memory and converting them into a unique and non-confusing representation of the memory becomes pattern separation (Buzsáki and Llinás, 2017).”
BackgroundSpatial memory requires hypocretins to elevate medial entorhinal gamma oscillations
Liao, Y., Wen, R., Fu, S., Cheng, X., Ren, S., Lu, M., Qian, L., Luo, F., Wang, Y., Xiao, Q., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.10.012 · Cited by 18 · see citing works
Hippocampal replay sequence governed by spontaneous brain-wide dynamics
Yang, Y., Leopold, D. A., Duyn, J. H., & Liu, X. (2024) · PNAS Nexus · doi:10.1093/pnasnexus/pgae078 · Cited by 19 · see citing works
“The embedding of hippocampal replays in the highly structured, resting-state global dynamics supports recent theory about the self-organized nature of the hippocampal neural sequences (12, 15, 20, 25).”
BackgroundLindeberg, T. (2023) · Biological Cybernetics · doi:10.1007/s00422-022-00953-6 · Cited by 17 · see citing works
“biological processes at multiple temporal scales (DeAngelis et al. 1995; DeAngelis andAnzai 2004; Gütig and Sompolinsky 2006; Gentner 2008; Holcombe 2009; Goldman 2009; Gauthier et al. 2012; Atencio and Schreiner 2012; Chait et al. 2015; Teng et al. 2016; Buzsáki and Llinás 2017; Tsao et al. 2018; Osman et al. 2018; L…”
Affective memory rehearsal with temporal sequences in amygdala neurons
Reitich-Stolero, T., & Paz, R. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0542-9 · Cited by 17 · see citing works
Spatiotemporal Psychopathology – A novel approach to brain and symptoms
Northoff, G. (2022) · Nöro Psikiyatri Arşivi · doi:10.29399/npa.28146 · Cited by 19 · see citing works
Long time-scales in primate amygdala neurons support aversive learning
Taub, A. H., Reitich-Stolero, T., Livneh, U., Shohat, Y., & Paz, R. (2018) · Nature Communications · doi:10.1038/s41467-018-07020-4 · Cited by 14 · see citing works
Phasic Neuronal Firing in the Rodent Nucleus of the Solitary Tract ex vivo
Chrobok, Ł., Wojcik, M., Klich, J. D., Pradel, K., Lewandowski, M. H., & Piggins, H. D. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.638695 · Cited by 16 · see citing works
Evolutionary origin and the development of consciousness
Александрович, К. И. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.034 · Cited by 15 · see citing works
“by thinking of some past event, we tend to not deal with the conceptualised proposition, but rather recollect a whole situation which contains rich experiential details (Buzsáki and Llinás, 2017).”
BackgroundPrefrontal cortical circuits in social behaviors: an overview
Cao, W., Li, H., & Luo, J. (2024) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b2300743 · Cited by 14 · see citing works
“Oscillations are hypothesized to create a temporal scaffold for intra-and inter-brain area communication (Buzsáki and Llinás, 2017).”
Calretinin+-neurons-mediated GABAergic inhibition in mouse prefrontal cortex
Saffari, R., Grotefeld, K., Kravchenko, M., Zhang, M., & Zhang, W. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109658 · Cited by 14 · see citing works
Hebbian learning revisited and its inference underlying cognitive function
Lim, S. (2021) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2021.02.006 · Cited by 14 · see citing works
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“…complexity on Alzheimer’s Disease via the mediation of spatial cognition and navigation despite the strong connections of spatial cognition and navigation to major categories of spatial cells in our hippocampal formation (27, 28) and furthermore to early cognitive symptoms of MCI and AD (10).”
BackgroundSemantic Knowledge Representation for Strategic Interactions in Dynamic Situations
Calvo, C., Villacorta-Atienza, J. A., Diez‐Hermano, S., Khoruzhko, M. A., Lobov, S. A., Potapov, I. A., Sánchez‐Jiménez, A., & Makarov, V. A. (2020) · Frontiers in Neurorobotics · doi:10.3389/fnbot.2020.00004 · Cited by 13 · see citing works
“Recently, a hypothesis that the brain entangles spatial and temporal dimensions in a single entity has been proposed (Villacorta-Atienza et al., 2010; Buzsaki and Llinas, 2017), which in the end gave rise to the GCM concept.”
BackgroundA momentum effect in temporal arithmetic
Bonato, M., D'Ovidio, U., Fias, W., & Zorzi, M. (2020) · Cognition · doi:10.1016/j.cognition.2020.104488 · Cited by 12 · see citing works
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Cross-Modal and Cognitive Processes in Sound Localization
Pastore, M. T., Zhou, Y., & Yost, W. A. (2020) · Modern acoustics and signal processing · doi:10.1007/978-3-030-00386-9_12 · Cited by 11 · see citing works
Fundamental Cause of Bio-Chirality: Space-Time Symmetry - Concept Review
Dyakin, V. V. (2022) · Symmetry · doi:10.3390/sym15010079 · Cited by 1 · see citing works
Learning to predict future locations with internally generated theta sequences
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Temporal Processing: Neural Correlates and Clinical Relevance
Lad, S. S., Hurley, R. A., & Taber, K. H. (2020) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.19120342 · Cited by 11 · see citing works
“Temporal perception (inner experience of time) is an abstract concept, constructed within the brain based on available information (external and internal sensory, memory) by a network of areas that likely are specialized for different aspects of timing (Figure 1 and Cover) (2, 3, 5 – 10).”
Minute-scale periodicity of neuronal firing in the human entorhinal cortex
Aghajan, Z. M., Kreiman, G., & Fried, I. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113271 · Cited by 12 · see citing works
Ma, M., de Souza, F. S., Futia, G. L., Anderson, S. R., Riguero, J., Tollin, D. J., Polese, A. G., Platt, J. P., Steinke, K., Hiratani, N., et al. (2024) · Current Biology · doi:10.1016/j.cub.2024.01.021 · Cited by 10 · see citing works
Sound-source localization as a multisystem process: The Wallach azimuth illusion
Yost, W. A., Pastore, M. T., & Pulling, K. R. (2019) · The Journal of the Acoustical Society of America · doi:10.1121/1.5116003 · Cited by 10 · see citing works
“Self-rotation is highly likely to involve proprioceptive, neural-motor control signals that could indicate head position (e.g., via efferent-copy processes; see Freeman et al., 2017; Yost et al., 2015, for explanations).”
BackgroundLessons From Astronomy and Biology for the Mind—Copernican Revolution in Neuroscience
Northoff, G. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00319 · Cited by 10 · see citing works
Cognitive Structures of Space-Time
Signorelli, C. M., Dündar‐Coecke, S., Wang, V., & Coecke, B. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2020.527114 · Cited by 10 · see citing works
Ghaderi, A. H. (2018) · Medical Hypotheses · doi:10.1016/j.mehy.2018.11.018 · Cited by 9 · see citing works
“However, just a few studies have addressed the relationship between subjective and physical time [3,2,12].”
BackgroundMultiplexing of temporal and spatial information in the lateral entorhinal cortex
Wang, C., Lee, H., Rao, G., & Knierim, J. J. (2024) · Nature Communications · doi:10.1038/s41467-024-54932-5 · Cited by 9 · see citing works
“The integration of space and time pro-cessinginLECandotherareassuggestsasharedorganizationalfeature across the MTL memory system 2,3,57,84 .”
Bonzon, P. E. (2019) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2019.00001 · Cited by 8 · see citing works
“Finally, Buzsaki and Llinas (2017) note that the neuronal mechanisms associated with navigation and memory are similar, meaning they process messages regardless of their origin.”
BackgroundPlace and Environment in the Ongoing Evolution of Cognitive Neuroscience
Irwin, L. N., & Irwin, B. A. (2020) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01607 · Cited by 8 · see citing works
“Buzsaki and Llinas (2017) noted that establishing a relationship between neuronal activity and distances in the world requires ambulation.”
BackgroundInfluentialMelcher, D., Kumar, D., & Srinivasan, N. (2020) · Scientific Reports · doi:10.1038/s41598-020-73830-6 · Cited by 8 · see citing works
Cerebellar Cortex 4–12 Hz Oscillations and Unit Phase Relation in the Awake Rat
Lévesque, M., Gao, H., Southward, C., Langlois, J. M. P., Léna, C., & Courtemanche, R. (2020) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2020.475948 · Cited by 8 · see citing works
Decoding Spatial Memory Retrieval in Cubical Space Using fMRI Signals
Guo, J., Zhang, K., Zhang, J., Zhao, R., Liang, Y., Lin, Y., Yu, S., Qin, W., & Yang, X. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.624352 · Cited by 8 · see citing works
“The way spatial memory is represented in the brain has been a motivating question for decades (Eichenbaum et al., 1999; Buzsaki and Llinas, 2017; Bellmund et al., 2018).”
BackgroundEbrahiminia, F., Cichy, R. M., & Khaligh‐Razavi, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.983602 · Cited by 8 · see citing works
“Any human cognitive function is realized by complex neural dynamics that evolve both in time and in locus (Haxby et al., 2014; Buzsáki and Llinás, 2017) across the brain.”
BackgroundKinds of individuals defined by patterns of variables
Kagan, J. (2018) · Development and Psychopathology · doi:10.1017/s095457941800055x · Cited by 5 · see citing works
“Buzsaki and Llinas (2017), however, reject the notion that neurons can represent fear or anxiety.”
BackgroundThe Emergent Engram: A Historical Legacy and Contemporary Discovery
Devan, B., Berger, K. D., & McDonald, R. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00168 · Cited by 8 · see citing works
“, the succession of events in neuronal activity (Buzsáki and Llinás, 2017).”
BackgroundLearning cognitive maps as structured graphs for vicarious evaluationPreprint
Rikhye, R. V., Gothoskar, N., Guntupalli, J. S., Dedieu, A., Lázaro-Gredilla, M., & George, D. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/864421 · Cited by 8 · see citing works
“the strong hypothesis that hippocampus performs a singular algorithm that learns a sequential, relational, content-agnostic structure, and demonstrated evidence for its validity [4].”
BackgroundProshina, E. A., Mitiureva, D. G., & Sysoeva, O. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1506987 · Cited by 7 · see citing works
White, P. A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105043 · Cited by 8 · see citing works
“There has been research on the encoding and representation of time, particularly involving the hippocampus (Bellmund et al., 2019; Buzsaki and Linas, 2017; Eichenbaum, 2017; Rolls and Mills, 2019; Sugar and Moser, 2019).”
Memory for the Future: Psychodynamic Approach to Time and Self Through the Default Network
Cieri, F. (2022) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.885315 · Cited by 8 · see citing works
Hippocampal place cells are topographically organized, but physical space has nothing to do with it
França, T. F. A., & Monserrat, J. M. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01968-9 · Cited by 7 · see citing works
Taxidis, J., Pnevmatikakis, E. A., Mylavarapu, A. L., Arora, J. S., Samadian, K. D., Hoffberg, E. A., & Golshani, P. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/474510 · Cited by 7 · see citing works
Temporal fingerprints of cortical gyrification in marmosets and humans
Wang, Q., Zhao, S., Liu, T., Han, J., & Liu, C. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad245 · Cited by 6 · see citing works
Physiological Adaptations to Life in Space: An Update
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Contiguity in perception: origins in cellular associative computations
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Sketching a Space of Brain States
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“While several studies investigate how space can be represented within the human brain [5], we are interested in finding how a brain can be represented within a conceptual space, as a parameter space.”
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“In order implement a detector of coincidence for handling messages (Buzsaki and Llinas, 2017), synaptic plasticity is abstracted through asynchronous communication protocols.”
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“The hippocampus integrates contextual cues, such as spatial or temporal information [480], allowing for a more precise encoding of the sequential relationships between events [113].”
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Same principle, but different computations in representing time and space
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- Authors
- Buzsáki, G., & Llinás, R.
- Affiliations
- New York University (US)
- Corresponding author
- Buzsáki, György
- ORCID
- Buzsáki, György
- Venue
- Science
- Published
- 2017-10-27
- Volume
- 358
- Issue
- 6362
- Pages
- 482-485
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC5998813
- OpenAlex
- W2766264103
- Semantic Scholar
- 492d4fdcadcc502d185bd3924176dbf422cf451a
- Cited by
- 175
- References
- 53
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 19 · 2023: 18 · 2022: 17 · 2021: 32 · 2020: 25 · 2019: 23 · 2018: 16 · 2017: 1 · 2015: 1
- FWCI
- 1.97
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (award343774, NS 090583, award343775, NS090526, award343777, NS074015)
- National Institute of Mental Health (award343773, MH54671)
- Simons Foundation (award343778)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Keywords
- spatial representation, representation of time, neuronal activity, navigation, memory, model development, inference
- MeSH terms
- Animals, Brain, Humans, Neurons, Space Perception, Time Perception, Rats, Memory, Episodic, Spatial Navigation
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