The hippocampal-striatal axis in learning, prediction and goal-directed behavior
Abstract
The hippocampal formation and striatum subserve declarative and procedural memory, respectively. However, experimental evidence suggests that the ventral striatum, as opposed to the dorsal striatum, does not lend itself to being part of either system. Instead, it may constitute a system integrating inputs from the amygdala, prefrontal cortex and hippocampus to generate motivational, outcome-predicting signals that invigorate goal-directed behaviors. Inspired by reinforcement learning models, we suggest an alternative scheme for computational functions of the striatum. Dorsal and ventral striatum are proposed to compute outcome predictions largely in parallel, using different types of information as input. The nature of the inputs to striatum is furthermore combinatorial, and the specificity of predictions transcends the level of scalar value signals, incorporating episodic information.
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The ventral striatum receives afferents from neural regions traditionally implicated in affective processes, including orbitofrontal cortex, dorsal anterior cingulate cortex, ventromedial PFC, amygdala, and hippocampus.
“The ventral striatum receives afferents from neural regions traditionally implicated in affective processes, including orbitofrontal cortex (OFC), dorsal anterior cingulate cortex, ventromedial PFC, amygdala, and hippocampus (e.g., Haber and Knutson, 2010, Pennartz et al., 2011; see Delgado, 2007).”
From Dopaminergic reward sensitivity can promote adolescent health: a new perspective on the mechanism of ventral striatum activation (2016) · cites this paper as Pennartz et al., 2011
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Functional organization of the hippocampal longitudinal axis
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Active Inference, homeostatic regulation and adaptive behavioural control
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“In a related perspective, these striatal territories might compute outcome predictions in parallel using different kinds of information as input (Pennartz et al., 2011).”
How prediction errors shape perception, attention, and motivation
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Reinforcement learning and episodic memory in humans and animals: an integrative framework
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Internally generated sequences in learning and executing goal-directed behavior
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Self-citationMemory trace replay: The shaping of memory consolidation by neuromodulation
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“Error signals incorporating model-based, highdimensional information (‘I got a banana instead of the apple I expected, but they are worth the same’) may involve cortical systems such as the anterior cingulate and orbitofrontal cortex, but also striatal regions [9,127,128] (see [31] for a more detailed computational an…”
BackgroundResultInfluentialIndicators and criteria of consciousness in animals and intelligent machines: an inside-out approach
Pennartz, C. M. A., Farisco, M., & Evers, K. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00025 · Cited by 121 · see citing works
Self-citationSocial rewards and social networks in the human brain
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Sleep and dreaming are for important matters
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“This off-line replay is induced by HC ripples and may be related to linking a memory trace to a motivational and emotional value during sleep (Lansink et al., 2009; Singer and Frank, 2009; Pennartz et al., 2011).”
BackgroundConsciousness, Representation, Action: The Importance of Being Goal-Directed
Pennartz, C. M. A. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.10.006 · Cited by 49 · see citing works
Self-citationThe principles of goal-directed decision-making: from neural mechanisms to computation and robotics
Pezzulo, G., Verschure, P. F. M. J., Balkenius, C., & Pennartz, C. M. A. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0470 · Cited by 35 · see citing works
Self-citationThe Surprising Role of the Default Mode Network
Brandman, T., Malach, R., & Simony., E. (2020) · doi:10.1101/2020.05.18.101758 · Cited by 88 · see citing works
- Authors
- Pennartz, C. M. A., Ito, R., Verschure, P. F. M. J., Battaglia, F. P., & Robbins, T. W.
- Affiliations
- University of Amsterdam (NL)
- University of Oxford (GB)
- Institució Catalana de Recerca i Estudis Avançats (ES)
- University of Cambridge (GB)
- Corresponding author
- Pennartz, C.M.A.
- Venue
- Trends in Neurosciences
- Publisher
- Elsevier BV
- Published
- 2011-10
- Volume
- 34
- Issue
- 10
- Pages
- 548-559
- ISSN
- 0166-2236 (ISSN-L)
- OpenAlex
- W2100983013
- Cited by
- 287
- References
- 154
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 20 · 2023: 10 · 2022: 26 · 2021: 24 · 2020: 14 · 2019: 17 · 2018: 30 · 2017: 13 · 2016: 24 · 2015: 24 · 2014: 30 · 2013: 15 · 2012: 22
- FWCI
- 1.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Trends in Neurosciences (publishedVersion)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Wellcome Trust (WT078197)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- ventral striatum, dorsal striatum, goal-directed behavior, outcome prediction, reinforcement learning, hippocampus, procedural memory, declarative memory
- MeSH terms
- Animals, Corpus Striatum, Goals, Hippocampus, Humans, Learning, Neural Pathways, Spatial Behavior
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