Anticipation and planning of future visual input require knowledge of the relational structure between events. The relational structure, for instance that stimulus B usually follows stimulus A, is learned through exposure during past experiences (Behrens et al., 2018; Finnie et al., 2021; Gavornik and Bear, 2014) and can be used to build a model or cognitive map (Tolman, 1948) that enables us to generate inferences in situation with noisy or partial input (Ekman et al., 2017; Momennejad, 2020; Schwartenbeck et al., 2021).

In the visual domain, with rapidly changing input, it remains unknown what the inherent properties of the model underlying our predictions are. On the one hand, such a model needs to be efficient enough to generate predictions from a constant stream of visual input, while on the other hand, it also allows for flexible updating in an ever-changing environment. In the context of hippocampal representations, the successor representation (SR) has been recently proposed (Dayan, 1993; Stachenfeld et al., 2017) to combine the trade-off between both flexible and efficient model properties. The SR postulates a predictive representation in which the current state is represented in terms of its future (successor) states, in a temporally discounted fashion. The SR is dependent on the actual experience, with states experienced more frequently being represented more strongly. This enables learning in an environment without explicit reward (Gläscher et al., 2010). This hypothesis captures many aspects of empirical hippocampal place cell firing pattern, like the exponential decay toward distant future locations (Alvernhe et al., 2011; Mehta et al., 2000).

Previous research has repeatedly shown that prior expectations influence neural activity in the visual cortex (Ekman et al., 2017; Gavornik and Bear, 2014; Hindy et al., 2016; Kok et al., 2012; Xu et al., 2012). It remains, however, unknown if SR-like representations are present outside the hippocampus in areas like the early visual cortex (V1) that have a strong retinotopic organization. Theoretically, it is possible that V1 receptive fields, analogous to hippocampal place fields, become tuned to respond not only to the current input, but also to expected future inputs. Here, we propose that the computationally efficient and flexible properties of the SR could in theory also underlie the anticipation of future events in V1.

To directly test this hypothesis, we conducted a functional magnetic resonance imaging (fMRI) study in which participants were presented with an arbitrary visual dot sequence (A-B-C-D). After initial sequence exposure, we introduced occasional omission trials, where only one element of the sequence was presented (e.g., B), while the rest of the sequence (e.g., A, C, and D) was omitted. These partial sequence trials allowed us to study expectations of future stimulus sequences in the absence of physical stimulation. This design allowed us to test the specific assumptions of the SR and also assess whether V1 predictions were better described by an alternative mechanism called pattern completion. Pattern completion describes a framework in which autoassociative connections within the hippocampal CA3 regions reactivate related sequence items from partial input (Deuker et al., 2014; Leutgeb and Leutgeb, 2007; Rolls, 2013) that is then propagated to sensory regions such as V1 (Hindy et al., 2016). In contrast to the SR, pattern completion predicts reactivations of all associated items, without any skewing toward future locations or temporal discounting of events that are farther in the future.

Using fMRI, we found reactivations of future sequence locations (e.g., C-D), but not of past locations (e.g., A) in both V1 and hippocampus. In line with the SR, a model comparison confirmed that predictive representations constitute a map-like structure, with exponential decay toward distant future states. Further, more detailed analysis of predictive codes revealed that hippocampus represented visual locations based on their temporal proximity within the sequence, rather than spatial distance.

Taken together, these data suggest that humans predict upcoming visual input by using a generative model whose properties resemble the SR. Importantly, the presence of SR-like representations in V1 indicates that SR might be a more ubiquitous coding schema that is present beyond hippocampal place cells. Finally, while SR-like representations were found to be present in both V1 and hippocampus, the predictive codes between these areas revealed complementary tuning properties, with hippocampus being sensitive to temporal distance and V1 being more sensitive to retinotopic spatial distance.

Human observers (N = 35) were exposed to four dots presented in rapid succession that formed an arbitrary visual sequence A-B-C-D (Figure 1A). Dot locations were sampled from eight locations (Figure 1B) and the resulting possible sequences were randomly assigned across subjects. After an initial exposure period with the full sequence (352 trials outside the scanner, 160 trials inside the scanner), occasionally only one item of the sequence was presented, omitting the remaining sequence items (e.g., partial sequence trial ‘- B - -’ where B is shown and A, C, and D are omitted; Figure 1A). Participants were instructed to maintain fixation throughout the experiment, and tasked to detect a slight temporal onset delay (170 ms vs. 17 ms) of the last sequence dot that occurred in ~40% of the full sequence trials. The task was designed to be demanding (group averaged hit rate = 78%, SD = 8%) and to keep participants’ attention on the sequence.

Figure 1

Download asset Open asset

We hypothesized that presenting only one item of the sequence would elicit anticipatory activity at the omitted sequence locations that followed the presented stimulus (i.e., successor states), but not at the sequence location that preceded the sequence item (i.e., predecessor states). For instance, during partial ‘- B - -’ trials, we expected activity at omitted sequence locations C (+1) and D (+2), but not at omitted location A (–1).

Stimulus sequences elicit spatially specific responses in V1

To test our prediction, we first selected V1 sub regions of interest (ROIs) that responded selectively to the eight stimulus locations based on an independent localizer session (Figure 1C). Stimulus-response profiles of these eight (retinotopic) ROIs show little coactivation of neighboring locations in the visual field which allows for a precise investigation of location-specific activity (Figure 2A). Unsurprisingly, during full sequence trials, BOLD activity at the sequence locations receiving bottom-up visual input was markedly enhanced compared to non-stimulated control locations (Figure 2B). Population-based receptive field (pRF) data that was acquired for a subset of participants confirmed that the selected voxels correspond to the retinotopic stimulus locations as expected. For all analyses, we subtracted the average BOLD activity of all control locations from the sequence location activity (Figure 3A), which provides an accurate measure of stimulus-specific responses independent of global signal fluctuations for instance due to attention.

Figure 2

Download asset Open asset

Figure 3

Download asset Open asset

Successor-like representation in V1

Next, we sought to formally test how well the observed data fits the prediction of the SR, namely an exponential decay of states farther into the future.

For each subject, we fitted partial sequence trials with an SR model (Figure 4A), keeping the exponential decay parameter γ as a free parameter (see Materials and methods). In order to evaluate how well the SR model resembled the data, we then computed the error between the SR prediction and the actual data (lower values indicate a better model fit). For comparison, we additionally fitted a traditional pattern-completion co-occurrence (CO) model that predicts that events that occur together, will be reactivated together (Figure 4B). In contrast to the SR model, predictions of the CO model are non-directional, meaning that it predicts equal reactivation of both successor and predecessor locations. Furthermore, while the SR model predicts a temporal discounting toward future states, the CO model assumes no differential activity of reactivated states. In our implementation of the CO model, anticipatory activity was modulated by one multiplicative parameter ω. Additionally, as a baseline model, we also evaluated a null model (H0) that assumes no predictive activity (i.e., no difference between successor and predecessor locations). Note that in order to be interpretable as a predictive representation, the best-fitting model should not only have the smallest error, but also differ significantly from the H0 model.

Figure 4

Download asset Open asset

Our results show that anticipatory activity in V1 is best described by the predictions of the SR (Figure 4C; SR vs. CO t(34) = –2.29, p = 0.028). Additionally, both SR and CO describe the data better than the null model (SR vs. H0 t(34) = –8.25, p = 1.24 × 10^–9; CO vs. H0: t test t(34) = –7.59, p = 8.22 × 10^–9).

SR in hippocampus

The predictive neural representation in the form of a SR was originally postulated for the hippocampus (Stachenfeld et al., 2017). We therefore wanted to investigate whether the predictive representations that we observed in V1 were also present in the hippocampus. Note that while the hippocampal formation and nearby entorhinal cortex might feature a coarse representation of visual space (Killian et al., 2012; Knapen, 2021; Nau et al., 2018b; Silson et al., 2020), it does not feature the same fine-scale retinotopic organization present in V1 (Dumoulin and Wandell, 2008). Therefore, instead of focusing on univariate BOLD activity within certain hippocampal subregions, we focused on population activity patterns across the entire hippocampus using a decoding approach similar to previous studies (Ekman et al., 2022; Kok and Turk-Browne, 2018; Kurth-Nelson et al., 2016; Russek et al., 2021; Schapiro et al., 2012).

In keeping with the V1 analysis, we used the independent stimulus localizer to extract location-specific activity patterns in the hippocampus and then tested during partial sequence trials to what extent location-specific representations were reactivated. Specifically, we trained a pattern classifier to distinguish between the eight dot locations within the localizer. Before applying the trained classifier to omission trials of the main task (see Materials and methods), we confirmed that cross-validated decoding accuracies within the localizer were above chance-level to ensure that the hippocampal pattern shows a reliable representation of space.

Within localizer decoding accuracy results confirmed that hippocampus has a coarse representation of the eight stimulus locations (Figure 5B) within the localizer (two-sided one-sample t test; t(34) = 3.28, p = 0.002; cross-validated accuracy = 15 ± 3.6%, mean ± s.d.; see Materials and methods). Notably, compared to V1 (Figure 2A), within localizer accuracy was relatively low and as a consequence tuning curves in hippocampus appeared less sharp (Figure 5C). In order to maximize sensitivity for the hippocampus, we averaged classification evidence across successor and predecessor locations. Non-averaged results can be found in Figure 5—figure supplement 1.

Figure 5 with 1 supplement see all

Download asset Open asset

Applying the trained classifier to partial sequence trials of the main task, we asked whether hippocampus would preferentially reactivate successor or predecessor locations (Figure 5D). To answer this question, we first subtracted the probabilistic classifier evidence for the control locations from the classifier evidence of the sequence locations. Consequently, values greater than 0 reflect evidence for the reactivation of sequence representations, while values smaller than 0 reflect a relative suppression of sequence locations. After that we averaged the evidence across all successor and predecessor locations, respectively, and tested for differences across participants. Our results reveal that hippocampus representations were preferentially biased toward successor locations (Figure 5E; paired-sample t test, t(34) = 2.74, p = 0.009), mirroring the results found in V1.

Finally, in order to better understand the temporal dynamics of the anticipatory representations in hippocampus, we repeated the decoding analysis in a time-resolved manner. We reasoned that if reactivations of future sequence locations were triggered by the brief presentations of partial sequence dots, the evidence time-course should follow a transient response profile. Alternatively, if hippocampus were to signal a constant bias toward future sequence locations, the evidence time-course should be unrelated to the stimulus onset and show a sustained temporal profile.

Results of the evidence difference time-course clearly show a transient response peaking approximately 4.7 s post-stimulus onset (Figure 5F) indicating that hippocampal predictions were triggered by the partial sequence dot. Note that the decoding time-course reflects the evidence for successor locations versus predecessor locations independent of the bottom-up stimulus. The transient decoding profile can therefore not simply reflect the onset of a given trial.

In order to probe the relationship between hippocampus and V1 successor reactivations, we performed an across-subject analysis, correlating V1 BOLD activity, averaged across all successor locations, with hippocampus classifier evidence, averaged across all successor locations. No significant relationship was observed (spearman correlation, r = –0.08, p = 0.668).

One could ask whether our findings are specific to V1 and hippocampus, or widespread throughout the brain. In order to answer this question, we repeated the analysis for low-level visual area V2. In contrast to V1, no predictive effects were found in area V2. V2 BOLD activity was not enhanced at the non-stimulated successor locations compared to the non-stimulated predecessor locations (averaged across all partial trials and sequence locations; t(34) = 1.41, p = 0.168).

Hippocampal codes preserve spatiotemporal tuning

In contrast to V1, hippocampal representations are not inherently retinotopic and feature only a coarse representation of visual space (Knapen, 2021; Nau et al., 2018b; Silson et al., 2021). Instead, hippocampal place cells provide a detailed representation of the allocentric position in an environment. However, more recently, the intriguing picture emerged that hippocampus also contributes to a more general organization of information by representing non-spatial aspects of experience in a map-like way (Constantinescu et al., 2016; Garvert et al., 2017; Stachenfeld et al., 2017), similar to the representation of space (Aronov et al., 2017).

Inspired by these recent observations, we asked what the underlying properties of the reported hippocampus representations were. Given that we successfully trained a classifier based on eight spatial locations, it might seem obvious to conclude that the underlying code for these representations is purely spatial (retinotopic) as well. This is however not necessarily the case, given that the localizer was shown after the main task and might therefore reflect persistent predictive representations. Instead, robust discrimination of sequence locations could theoretically also be based on coding of temporal properties of the sequence. Indeed, Deuker et al., 2016 have recently shown that hippocampus representations can reflect in principle both spatial and temporal aspects. In our case, a temporal coding mechanism could represent stimulus locations not based on proximity in space, but rather by proximity in time.

In order to address this question, we conducted a detailed analysis of the coactivation pattern in the stimulus localizer (Figure 6A). Note that the localizer was shown at the end of the study, allowing us to test whether learned associations persisted even after the full sequence was not relevant anymore. Here, coactivations were defined as activation of non-stimulated locations. For instance, when presenting stimulus A, locations B-C-D might become activated as well. In general, such coactivations are often attributed to noise or ambivalent responses driven by overlapping receptive fields. However, in this case, we made use of the coactivation pattern to draw inferences about the learned persistent representations.

Figure 6

Download asset Open asset

Specifically, for a representation based on spatial coactivation (tuning) one would expect a coactivation of nearby spatial locations. In other words, the coactivation of non-stimulated locations should be modulated by the spatial (Euclidean) distance to the stimulated location (Figure 6B). This spatial tuning pattern is typically seen in early visual areas with overlapping receptive fields and is also visually present in our V1 results (Figure 2A). Alternatively, for a representation based on temporal coactivation (tuning) one would expect a coactivation of nearby locations in sequence space (Figure 6C).

Thus, spatial and temporal tuning codes lead to different coactivation patterns (Figure 6D) that can be disentangled with our stimulus paradigm. For instance, sequence locations A and B were far apart in the spatial (Euclidean) domain, but close in the temporal domain (distance in sequence space). Conversely, locations A and D are close in terms of spatial distance, but far apart in terms of temporal distance (Figure 6B). Note, while spatial tuning is in principle independent of any task-specific experience, temporal tuning on the other hand requires exposure to a sequential structure and can therefore only occur for the four dots that were part of the sequence. For this reason, we restricted the coactivation (tuning) analysis to the four dot locations that were part of the sequence.

For each participant, individual localizer data were fitted by a spatial coactivation model, a temporal coactivation model, an SR model, and a no-coactivation (H0) control model (Figure 6D). The latter was included as a low-level baseline control. Visual inspection of the group averaged localizer coactivation pattern revealed a clear temporal tuning pattern in hippocampus but not in V1 (Figure 6E). These results were confirmed by a formal model comparison (Figure 6F, Hippocampus: two-sided t test, Temporal vs. Spatial t(34) = −2.36, p = 0.024; Temporal vs. SR t(34) = −3.24, p = 0.003; Temporal vs. H0 t(34) = −19.27, p = 7.12 × 10^–20; V1: H0 vs. Temporal t(34) = −22.09, p = 9.49 × 10^–22; H0 vs. Spatial t(34) = −14.26, p = 6.52 × 10^–16; H0 vs. SR t(34) = −17.15, p = 2.61 × 10^–18).

Uncovering the computations that drive human prediction and planning is a central aspect when it comes to understanding human cognition. What are the general coding mechanisms that allow to utilize knowledge of the environment to make inferences and generalizations about future events? In this study, we sought to answer the question whether the map-like SR that has been posited for the hippocampus (Mehta et al., 2000; Stachenfeld et al., 2017) may also explain the shape of anticipatory activity in visual cortex (V1).

There is an extensive body of literature that shows how expectations elicit anticipatory activity in early visual cortices (de Lange et al., 2018; Hindy et al., 2016; Kok et al., 2012). For instance, we have previously shown that flashing an individual dot of a simple, linear sequence triggers an activity wave in V1 that resembles the full stimulus sequence (Ekman et al., 2017; Ekman et al., 2022), akin to replay of place field activity during spatial navigation (Foster and Wilson, 2006; Gupta et al., 2010). However, what remains unknown is whether these sensory replay traces are guided by a generative model that represents the relational structure of the stimulus sequence, akin to a predictive map. Alternatively, anticipatory activity traces could simply reflect the association between different stimuli, based on their CO, without the added complexity of any temporal relational structure. The latter explanation appears plausible, given that predictive representations in early visual cortex are generally time critical and operate in parallel to a constant stream of new sensory input, which arguably requires efficient processing and in turn limits the complexity of such representations.

In fact, we previously speculated that cue-triggered reactivation of simple sequences might be driven by an automatic pattern completion-like mechanism that reactivates all associated items based on partial input (Ekman et al., 2017). This idea is in line with the finding that predictive representations in V1 correlated with pattern completion-like activity in the hippocampus (Hindy et al., 2016; Kok and Turk-Browne, 2018) that might be driving V1 activity (Finnie et al., 2021; Ji and Wilson, 2007).

Our current findings directly challenge this interpretation and instead point to a predictive representation of expected, temporally discounted, future states. We accomplished this by using a paradigm in which one visual event (e.g., the presentation of one dot) was framed as one state in a directed transition matrix with a fixed relational structure. The SR hypothesis makes two testable predictions, namely that population activity represents future states over predecessor states, and that future state representations are temporally discounted, such that events in the close future are more prominently represented compared to events in the distant future. Using a paradigm in which we occasionally presented only single items of the full sequence, allowed us to investigate V1 activity at omitted sequence locations.

Confirming the SR predictions, V1 activity at the successor locations was enhanced compared to activity at the predecessor locations, indicating a representation skewed toward future locations and away from the past. Notably, this relative difference was not only due to an enhancement of successor states, but our results also showed a decrease of activity at the predecessor states (compared to baseline). This suppression of predecessor states might seem surprising at first given that SR postulates the mere absence of predecessor activity (Momennejad, 2020; Stachenfeld et al., 2017). We speculate that the observed decrease at the predecessor states might constitute a functional separation mechanism between predecessor and successor states, strengthening the future-directed representation of the sequence by selectively decreasing representations of the unexpected predecessor states.

One aspect that sets our study apart is that the viewing of the visual sequence does not require any predictive planning of the participant to evaluate different future outcomes. In contrast, related studies reporting neuronal evidence for SR-like representations in hippocampus and PFC (Barron et al., 2020; Brunec and Momennejad, 2022) and occipital cortex (Schwartenbeck et al., 2021) have used paradigms in which participants were actively engaged in prospective planning and choice evaluation. Given the relatively passive nature of our task, one might therefore wonder whether it is expected to find any map-like activity at all. However, in this context, it is important to stress that the SR, unlike other model-based algorithms, does not depend on choice-dependent reward to build its transitional task structure (Momennejad et al., 2017; Stachenfeld et al., 2017) and therefore might not depend on participants’ active engagement. Furthermore, Russek et al., 2021 have recently used a paradigm in which subjects were passively exposed to transitions between visual states and reported evidence for SR-like representations in the absence of active choices in line with the results of the present study. Further supporting this notion, we have previously shown that anticipatory sequence activity occurred even after subjects’ attention was diverted from the sequence to a demanding task at fixation (Ekman et al., 2017), rendering the sequence task irrelevant. Taken together, these observations indicate that SR-like representations are not limited to situations that require active planning, or multiple-choice evaluations but may rather be formed automatically and incidentally, as has been shown repeatedly in the domain of statistical learning (Fiser and Aslin, 2002; Turk-Browne et al., 2005).

While we have interpreted the neural activity patterns in the light of the SR, it is strictly speaking not possible to distinguish between model-based (MB) and SR algorithms within the context of our design. The key distinction between them is that SR caches a predictive map of states that the agent expects to visit in the future, whereas MB algorithms store a full model of the world and compute trajectories at the decision time (Gershman, 2018; Momennejad et al., 2017). Therefore, both predict a temporally discounted activation of successor states. It should be noted however that MB comes at a higher computational cost, and is more intensive both in terms of time and working memory resources. The activation of successor states that we observed, on the other hand, occurred in the absence of a decision-making process (i.e., participants did not perform any task on the trials where a single dot was presented). Also, importantly, we previously observed that this activation pattern was not dependent on the task, and was equally present when attentional resources were strongly drawn away from the stimuli (Ekman et al., 2017). These observations may be more readily in line with the automatic (cached) activation of successor states that is embodied by SR, rather than the effortful iterative calculation of successor states that is the hallmark of MB. One future possibility to disentangle SR and MB algorithms could be to probe how well each model adapts to changes in the dot sequence structure. It has previously been shown, that compared to MB, the flexibility of the SR is somewhat limited to reflect changes in the transitional structure, because it requires the entire SR to be relearned (Momennejad et al., 2018).

The hippocampal formation can acquire arbitrary relationships between objects (Aronov et al., 2017; Backus et al., 2016; Behrens et al., 2018; Constantinescu et al., 2016; Garvert et al., 2017) beyond geometric location in space (O’Keefe and Nadel, 1978). While our main focus in the current study was on V1 representations, we also wanted to test to what extent hippocampus showed a similar SR-like representation of visual sequences. Previous fMRI studies investigating hippocampal representations have mainly focused on either navigation in a spatial (Brunec and Momennejad, 2022; Deuker et al., 2016) or non-spatial task (Garvert et al., 2017; Schapiro et al., 2013; Schuck and Niv, 2019) in which participants explore a relatively complex task space. It was recently shown that hippocampus has a rudimentary representation of visual space (Knapen, 2021; Silson et al., 2021), but it was not clear whether hippocampus would also engage in the representation of a comparably simple, low-level visual sequence presented in our paradigm.

Our results confirmed that hippocampus representations resemble an SR-like predictive map, favoring future over past sequence locations. This result highlights the compelling conceptual parallels between mnemonic expectations in hippocampus (Hindy et al., 2016) and its perceptual manifestation in sensory cortex. On a conceptual level, navigation (in memory and space) and processing visual events both involve abstraction of the relational structure between events to enable forward planning and predictions. Similar to navigational space, visual space can be represented in terms of its relational structure-like direction and distance, and it has been suggested that similar mechanisms might underlie spatial and non-spatial representations (Nau et al., 2018a), especially if there is sequential structure present (Finnie et al., 2021). Supporting this notion, recently, a conceptual link between representations for visual understanding and spatial navigation has been proposed that suggests a common underlying map-like representation of visual and navigational task structure (Schwartenbeck et al., 2021).

These conceptual links, as well as anatomical (Felleman and Van Essen, 1991; Huang et al., 2021) and functional connections between the hippocampus and visual cortex (Bosch et al., 2014; Hindy et al., 2016; Ji and Wilson, 2007; Kok and Turk-Browne, 2018; Lee et al., 2012; Nau et al., 2018a) raise the question whether hippocampal representations are independent from V1, or whether V1 is instead receiving the predictions as a feedback signal from hippocampus. Supporting the idea of functional feedback, Finnie et al., 2021 recently showed that V1 predictions were heavily impaired after hippocampus damage. However, contrary to this notion, spatiotemporal sequence predictions have also been shown to occur locally within V1 without the need for top-down predictions (Gavornik and Bear, 2014; Xu et al., 2012). Our study showed no functional relationship between sequence prediction in V1 and hippocampus. However, our experimental paradigm was not primarily designed to address this question, as it does not exclude the possibility that an apparent coordination might be driven by other factors like attentional fluctuations across participants. Further, V1-hippocampus coordination might exist on a trial-by-trial level, which does not necessarily transfer to statistical comparisons across participants. Future experiments, using more than one stimulus sequence could potentially address this question by comparing evidence of sequence-specific representations in both areas within participants.

It is notable that while hippocampal and visual representations appear similar with respect to their SR-like representation, they also show qualitative differences with respect to their underlying coding properties. V1 representations of individual sequence items resembled a coding based on spatial tuning. Hippocampus on the other hand represented relevant items predominantly in terms of their temporal distance within the sequence, suggesting that representations capitulate on the transitionally structure of the visual sequence. These results align with previous reports that hippocampus can learn to represent temporal sequence structure (Thavabalasingam et al., 2018; Thavabalasingam et al., 2019) and temporal proximity in a spatial navigation task (Deuker et al., 2016; Howard et al., 2014), but to the best of our knowledge, constitute the first reports of coding temporal distance of a visual sequence.

Furthermore, hippocampus predictive codes were found to persist after the sequence task and coactivation of related sequence locations was still present during the stimulus localizer, potentially indicating that hippocampus representations reflect a more stable code operating on a longer timescale. V1 representations on the other hand did not persist throughout the stimulus localizer and reverted back to representing individual spatial locations without coactivation of related sequence locations, further highlighting another qualitative difference between V1 and hippocampus coding. According to the SR, it is expected that sequence predictions will change once the regularities of the environment change. The absence of SR-like pattern in V1 during the functional localizer is therefore not at odds with our results from the main task, but rather indicative of a dynamic updating of the generative model. Taken these qualitative differences together, it is reasonable to speculate that predictive activity in V1 does not merely reflect top-down feedback from hippocampus, but instead that SR-like representations in V1 are somewhat independent, and potentially complementary, to SR-like representations found in the hippocampus.

In conclusion, our data show that anticipatory activity in early visual cortex and hippocampus is guided by a generative model that represents the relational structure of the visual world, akin to a predictive map. Our results suggest that the observed SR-like representation underlying visual predictions can provide a sophisticated state space representation that enables flexible generalization from partial input to future sequence locations, while also being efficient enough to provide rapid visual computations.

All data and code used for stimulus presentation and analysis are available on the Donders Repository (https://doi.org/10.34973/bsy6-9h29).

1. 1. Ekman M
   2. Kusch S
   3. de Lange FP

   (2023) Donders Repository

   Successor-like representation guides the prediction of future events in human visual cortex and hippocampus.

   https://doi.org/10.34973/bsy6-9h29

1. 1. Alvernhe A
   2. Save E
   3. Poucet B

   (2011) Local remapping of place cell firing in the tolman detour task

   The European Journal of Neuroscience 33:1696–1705.

   https://doi.org/10.1111/j.1460-9568.2011.07653.x

   • PubMed
   • Google Scholar
2. 1. Aronov D
   2. Nevers R
   3. Tank DW

   (2017) Mapping of a non-spatial dimension by the hippocampal-entorhinal circuit

   Nature 543:719–722.

   https://doi.org/10.1038/nature21692

   • PubMed
   • Google Scholar
3. 1. Backus AR
   2. Bosch SE
   3. Ekman M
   4. Grabovetsky AV
   5. Doeller CF

   (2016) Mnemonic convergence in the human hippocampus

   Nature Communications 7:11991.

   https://doi.org/10.1038/ncomms11991

   • PubMed
   • Google Scholar
4. 1. Barron HC
   2. Reeve HM
   3. Koolschijn RS
   4. Perestenko PV
   5. Shpektor A
   6. Nili H
   7. Rothaermel R
   8. Campo-Urriza N
   9. O’Reilly JX
   10. Bannerman DM
   11. Behrens TEJ
   12. Dupret D

   (2020) Neuronal computation underlying inferential reasoning in humans and mice

   Cell 183:228–243.

   https://doi.org/10.1016/j.cell.2020.08.035

   • PubMed
   • Google Scholar
5. 1. Behrens TEJ
   2. Muller TH
   3. Whittington JCR
   4. Mark S
   5. Baram AB
   6. Stachenfeld KL
   7. Kurth-Nelson Z

   (2018) What is a cognitive map

   Organizing Knowledge for Flexible Behavior. Neuron 100:490–509.

   https://doi.org/10.1016/j.neuron.2018.10.002

   • Google Scholar
6. 1. Bosch SE
   2. Jehee JFM
   3. Fernández G
   4. Doeller CF

   (2014) Reinstatement of associative memories in early visual cortex is signaled by the hippocampus

   The Journal of Neuroscience 34:7493–7500.

   https://doi.org/10.1523/JNEUROSCI.0805-14.2014

   • PubMed
   • Google Scholar
7. 1. Brunec IK
   2. Momennejad I

   (2022) Predictive representations in hippocampal and prefrontal hierarchies

   The Journal of Neuroscience 42:299–312.

   https://doi.org/10.1523/JNEUROSCI.1327-21.2021

   • PubMed
   • Google Scholar
8. 1. Constantinescu AO
   2. O’Reilly JX
   3. Behrens TEJ

   (2016) Organizing conceptual knowledge in humans with a gridlike code

   Science 352:1464–1468.

   https://doi.org/10.1126/science.aaf0941

   • PubMed
   • Google Scholar
9. 1. Dayan P

   (1993) Improving generalization for temporal difference learning: the successor representation

   Neural Computation 5:613–624.

   https://doi.org/10.1162/neco.1993.5.4.613

   • Google Scholar
10. 1. de Lange FP
    2. Heilbron M
    3. Kok P

    (2018) How do expectations shape perception?

    Trends in Cognitive Sciences 22:764–779.

    https://doi.org/10.1016/j.tics.2018.06.002

    • PubMed
    • Google Scholar
11. 1. Deuker L
    2. Doeller CF
    3. Fell J
    4. Axmacher N

    (2014) Human neuroimaging studies on the hippocampal CA3 region - integrating evidence for pattern separation and completion

    Frontiers in Cellular Neuroscience 8:64.

    https://doi.org/10.3389/fncel.2014.00064

    • PubMed
    • Google Scholar
12. 1. Deuker L
    2. Bellmund JL
    3. Navarro Schröder T
    4. Doeller CF

    (2016) An event map of memory space in the hippocampus

    eLife 5:e16534.

    https://doi.org/10.7554/eLife.16534

    • PubMed
    • Google Scholar
13. 1. Dumoulin SO
    2. Wandell BA

    (2008) Population receptive field estimates in human visual cortex

    NeuroImage 39:647–660.

    https://doi.org/10.1016/j.neuroimage.2007.09.034

    • PubMed
    • Google Scholar
14. 1. Ekman M
    2. Kok P
    3. de Lange FP

    (2017) Time-compressed preplay of anticipated events in human primary visual cortex

    Nature Communications 8:15276.

    https://doi.org/10.1038/ncomms15276

    • PubMed
    • Google Scholar
15. Preprint

    1. Ekman M
    2. Gennari G
    3. de Lange FP

    (2022) Probabilistic Forward Replay of Anticipated Stimulus Sequences in Human Primary Visual Cortex and Hippocampus

    bioRxiv.

    https://doi.org/10.1101/2022.01.26.477907

    • Google Scholar
16. 1. Felleman DJ
    2. Van Essen DC

    (1991) Distributed hierarchical processing in the primate cerebral cortex

    Cerebral Cortex 1:1–47.

    https://doi.org/10.1093/cercor/1.1.1-a

    • PubMed
    • Google Scholar
17. 1. Finnie PSB
    2. Komorowski RW
    3. Bear MF

    (2021) The spatiotemporal organization of experience dictates hippocampal involvement in primary visual cortical plasticity

    Current Biology 31:3996–4008.

    https://doi.org/10.1016/j.cub.2021.06.079

    • PubMed
    • Google Scholar
18. 1. Fischl B

    (2012) FreeSurfer

    NeuroImage 62:774–781.

    https://doi.org/10.1016/j.neuroimage.2012.01.021

    • PubMed
    • Google Scholar
19. 1. Fiser J
    2. Aslin RN

    (2002) Statistical learning of higher-order temporal structure from visual shape sequences

    Journal of Experimental Psychology. Learning, Memory, and Cognition 28:458–467.

    https://doi.org/10.1037//0278-7393.28.3.458

    • PubMed
    • Google Scholar
20. 1. Foster DJ
    2. Wilson MA

    (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state

    Nature 440:680–683.

    https://doi.org/10.1038/nature04587

    • PubMed
    • Google Scholar
21. 1. Garvert MM
    2. Dolan RJ
    3. Behrens TE

    (2017) A map of abstract relational knowledge in the human hippocampal-entorhinal cortex

    eLife 6:e17086.

    https://doi.org/10.7554/eLife.17086

    • PubMed
    • Google Scholar
22. 1. Gavornik JP
    2. Bear MF

    (2014) Learned spatiotemporal sequence recognition and prediction in primary visual cortex

    Nature Neuroscience 17:732–737.

    https://doi.org/10.1038/nn.3683

    • PubMed
    • Google Scholar
23. 1. Gershman SJ

    (2018) The successor representation: its computational logic and neural substrates

    The Journal of Neuroscience 38:7193–7200.

    https://doi.org/10.1523/JNEUROSCI.0151-18.2018

    • PubMed
    • Google Scholar
24. 1. Gläscher J
    2. Daw N
    3. Dayan P
    4. O’Doherty JP

    (2010) States versus rewards: dissociable neural prediction error signals underlying model-based and model-free reinforcement learning

    Neuron 66:585–595.

    https://doi.org/10.1016/j.neuron.2010.04.016

    • PubMed
    • Google Scholar
25. 1. Gupta AS
    2. van der Meer MAA
    3. Touretzky DS
    4. Redish AD

    (2010) Hippocampal replay is not a simple function of experience

    Neuron 65:695–705.

    https://doi.org/10.1016/j.neuron.2010.01.034

    • PubMed
    • Google Scholar
26. 1. Hindy NC
    2. Ng FY
    3. Turk-Browne NB

    (2016) Linking pattern completion in the hippocampus to predictive coding in visual cortex

    Nature Neuroscience 19:665–667.

    https://doi.org/10.1038/nn.4284

    • PubMed
    • Google Scholar
27. 1. Howard LR
    2. Javadi AH
    3. Yu Y
    4. Mill RD
    5. Morrison LC
    6. Knight R
    7. Loftus MM
    8. Staskute L
    9. Spiers HJ

    (2014) The hippocampus and entorhinal cortex encode the path and euclidean distances to goals during navigation

    Current Biology 24:1331–1340.

    https://doi.org/10.1016/j.cub.2014.05.001

    • PubMed
    • Google Scholar
28. 1. Huang CC
    2. Rolls ET
    3. Hsu CCH
    4. Feng J
    5. Lin CP

    (2021) Extensive cortical connectivity of the human hippocampal memory system: beyond the “ what” and “ where” dual stream model

    Cerebral Cortex 31:4652–4669.

    https://doi.org/10.1093/cercor/bhab113

    • PubMed
    • Google Scholar
29. 1. Ji D
    2. Wilson MA

    (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep

    Nature Neuroscience 10:100–107.

    https://doi.org/10.1038/nn1825

    • PubMed
    • Google Scholar
30. 1. Kay KN
    2. Weiner KS
    3. Grill-Spector K

    (2015) Attention reduces spatial uncertainty in human ventral temporal cortex

    Current Biology 25:595–600.

    https://doi.org/10.1016/j.cub.2014.12.050

    • PubMed
    • Google Scholar
31. 1. Killian NJ
    2. Jutras MJ
    3. Buffalo EA

    (2012) A map of visual space in the primate entorhinal cortex

    Nature 491:761–764.

    https://doi.org/10.1038/nature11587

    • PubMed
    • Google Scholar
32. 1. Klink PC
    2. Chen X
    3. Vanduffel W
    4. Roelfsema PR

    (2021) Population receptive fields in nonhuman primates from whole-brain fmri and large-scale neurophysiology in visual cortex

    eLife 10:e67304.

    https://doi.org/10.7554/eLife.67304

    • PubMed
    • Google Scholar
33. 1. Knapen T

    (2021) Topographic connectivity reveals task-dependent retinotopic processing throughout the human brain

    PNAS 118:e2017032118.

    https://doi.org/10.1073/pnas.2017032118

    • PubMed
    • Google Scholar
34. 1. Kok P
    2. Jehee JFM
    3. de Lange FP

    (2012) Less is more: expectation sharpens representations in the primary visual cortex

    Neuron 75:265–270.

    https://doi.org/10.1016/j.neuron.2012.04.034

    • PubMed
    • Google Scholar
35. 1. Kok P
    2. Turk-Browne NB

    (2018) Associative prediction of visual shape in the hippocampus

    The Journal of Neuroscience 38:6888–6899.

    https://doi.org/10.1523/JNEUROSCI.0163-18.2018

    • PubMed
    • Google Scholar
36. 1. Kurth-Nelson Z
    2. Economides M
    3. Dolan RJ
    4. Dayan P

    (2016) Fast sequences of non-spatial state representations in humans

    Neuron 91:194–204.

    https://doi.org/10.1016/j.neuron.2016.05.028

    • PubMed
    • Google Scholar
37. 1. Lee ACH
    2. Yeung LK
    3. Barense MD

    (2012) The hippocampus and visual perception

    Frontiers in Human Neuroscience 6:91.

    https://doi.org/10.3389/fnhum.2012.00091

    • PubMed
    • Google Scholar
38. 1. Leutgeb S
    2. Leutgeb JK

    (2007) Pattern separation, pattern completion, and new neuronal codes within a continuous CA3 MAP

    Learning & Memory 14:745–757.

    https://doi.org/10.1101/lm.703907

    • PubMed
    • Google Scholar
39. 1. Mehta MR
    2. Quirk MC
    3. Wilson MA

    (2000) Experience-dependent asymmetric shape of hippocampal receptive fields

    Neuron 25:707–715.

    https://doi.org/10.1016/s0896-6273(00)81072-7

    • PubMed
    • Google Scholar
40. 1. Moeller S
    2. Yacoub E
    3. Olman CA
    4. Auerbach E
    5. Strupp J
    6. Harel N
    7. Uğurbil K

    (2010) Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fmri

    Magnetic Resonance in Medicine 63:1144–1153.

    https://doi.org/10.1002/mrm.22361

    • PubMed
    • Google Scholar
41. 1. Momennejad I
    2. Russek EM
    3. Cheong JH
    4. Botvinick MM
    5. Daw ND
    6. Gershman SJ

    (2017) The successor representation in human reinforcement learning

    Nature Human Behaviour 1:680–692.

    https://doi.org/10.1038/s41562-017-0180-8

    • Google Scholar
42. 1. Momennejad I
    2. Otto AR
    3. Daw ND
    4. Norman KA

    (2018) Offline replay supports planning in human reinforcement learning

    eLife 7:e32548.

    https://doi.org/10.7554/eLife.32548

    • PubMed
    • Google Scholar
43. 1. Momennejad I

    (2020) Learning structures: predictive representations, replay, and generalization

    Current Opinion in Behavioral Sciences 32:155–166.

    https://doi.org/10.1016/j.cobeha.2020.02.017

    • PubMed
    • Google Scholar
44. 1. Nau M
    2. Julian JB
    3. Doeller CF

    (2018a) How the brain’s navigation system shapes our visual experience

    Trends in Cognitive Sciences 22:810–825.

    https://doi.org/10.1016/j.tics.2018.06.008

    • PubMed
    • Google Scholar
45. 1. Nau M
    2. Navarro Schröder T
    3. Bellmund JLS
    4. Doeller CF

    (2018b) Hexadirectional coding of visual space in human entorhinal cortex

    Nature Neuroscience 21:188–190.

    https://doi.org/10.1038/s41593-017-0050-8

    • PubMed
    • Google Scholar
46. Book

    1. O’Keefe J
    2. Nadel L

    (1978)

    The Hippocampus as a Cognitive Map

    Clarendon Press.

    • Google Scholar
47. 1. Pedregosa F
    2. Varoquaux G
    3. Gramfort A
    4. Michel V
    5. Thirion B
    6. Grisel O
    7. Blondel M
    8. Prettenhofer P
    9. Weiss R
    10. Dubourg V
    11. Vanderplas J
    12. Passos A
    13. Cournapeau D
    14. Brucher M
    15. Perrot M
    16. Duchesnay É

    (2011)

    Scikit-learn: machine learning in python

    Journal of Machine Learning Research 12:2825–2830.

    • Google Scholar
48. 1. Rolls ET

    (2013) The mechanisms for pattern completion and pattern separation in the hippocampus

    Frontiers in Systems Neuroscience 7:74.

    https://doi.org/10.3389/fnsys.2013.00074

    • PubMed
    • Google Scholar
49. Preprint

    1. Russek EM
    2. Momennejad I
    3. Botvinick MM
    4. Gershman SJ
    5. Daw ND

    (2021) Neural Evidence for the Successor Representation in Choice Evaluation

    bioRxiv.

    https://doi.org/10.1101/2021.08.29.458114

    • Google Scholar
50. 1. Savitzky A
    2. Golay MJE

    (1964) Smoothing and differentiation of data by simplified least squares procedures

    Analytical Chemistry 36:1627–1639.

    https://doi.org/10.1021/ac60214a047

    • Google Scholar
51. 1. Schapiro AC
    2. Kustner LV
    3. Turk-Browne NB

    (2012) Shaping of object representations in the human medial temporal lobe based on temporal regularities

    Current Biology 22:1622–1627.

    https://doi.org/10.1016/j.cub.2012.06.056

    • PubMed
    • Google Scholar
52. 1. Schapiro AC
    2. Rogers TT
    3. Cordova NI
    4. Turk-Browne NB
    5. Botvinick MM

    (2013) Neural representations of events arise from temporal community structure

    Nature Neuroscience 16:486–492.

    https://doi.org/10.1038/nn.3331

    • PubMed
    • Google Scholar
53. 1. Schuck NW
    2. Niv Y

    (2019) Sequential replay of nonspatial task states in the human hippocampus

    Science 364:eaaw5181.

    https://doi.org/10.1126/science.aaw5181

    • PubMed
    • Google Scholar
54. Preprint

    1. Schwartenbeck P
    2. Baram A
    3. Liu Y
    4. Mark S
    5. Muller T
    6. Dolan R
    7. Botvinick M
    8. Kurth-Nelson Z
    9. Behrens T

    (2021) Generative Replay for Compositional Visual Understanding in the Prefrontal-Hippocampal Circuit

    bioRxiv.

    https://doi.org/10.1101/2021.06.06.447249

    • Google Scholar
55. Preprint

    1. Silson EH
    2. Zeidman P
    3. Knapen T
    4. Baker CI

    (2020) Representation of Contralateral Visual Space in the Human Hippocampus

    bioRxiv.

    https://doi.org/10.1101/2020.07.30.228361

    • Google Scholar
56. 1. Silson EH
    2. Zeidman P
    3. Knapen T
    4. Baker CI

    (2021) Representation of contralateral visual space in the human hippocampus

    The Journal of Neuroscience 41:2382–2392.

    https://doi.org/10.1523/JNEUROSCI.1990-20.2020

    • PubMed
    • Google Scholar
57. 1. Smith SM
    2. Jenkinson M
    3. Woolrich MW
    4. Beckmann CF
    5. Behrens TEJ
    6. Johansen-Berg H
    7. Bannister PR
    8. De Luca M
    9. Drobnjak I
    10. Flitney DE
    11. Niazy RK
    12. Saunders J
    13. Vickers J
    14. Zhang Y
    15. De Stefano N
    16. Brady JM
    17. Matthews PM

    (2004) Advances in functional and structural mr image analysis and implementation as fsl

    NeuroImage 23:S208–S219.

    https://doi.org/10.1016/j.neuroimage.2004.07.051

    • Google Scholar
58. 1. Stachenfeld KL
    2. Botvinick MM
    3. Gershman SJ

    (2017) The hippocampus as a predictive MAP

    Nature Neuroscience 20:1643–1653.

    https://doi.org/10.1038/nn.4650

    • PubMed
    • Google Scholar
59. 1. Thavabalasingam S
    2. O’Neil EB
    3. Lee ACH

    (2018) Multivoxel pattern similarity suggests the integration of temporal duration in hippocampal event sequence representations

    NeuroImage 178:136–146.

    https://doi.org/10.1016/j.neuroimage.2018.05.036

    • PubMed
    • Google Scholar
60. 1. Thavabalasingam S
    2. O’Neil EB
    3. Tay J
    4. Nestor A
    5. Lee ACH

    (2019) Evidence for the incorporation of temporal duration information in human hippocampal long-term memory sequence representations

    PNAS 116:6407–6414.

    https://doi.org/10.1073/pnas.1819993116

    • Google Scholar
61. 1. Tolman EC

    (1948) Cognitive maps in rats and men

    Psychological Review 55:189–208.

    https://doi.org/10.1037/h0061626

    • PubMed
    • Google Scholar
62. 1. Turk-Browne NB
    2. Jungé JA
    3. Scholl BJ

    (2005) The automaticity of visual statistical learning

    Journal of Experimental Psychology. General 134:552–564.

    https://doi.org/10.1037/0096-3445.134.4.552

    • PubMed
    • Google Scholar
63. 1. Virtanen P
    2. Gommers R
    3. Oliphant TE
    4. Haberland M
    5. Reddy T
    6. Cournapeau D
    7. Burovski E
    8. Peterson P
    9. Weckesser W
    10. Bright J
    11. van der Walt SJ
    12. Brett M
    13. Wilson J
    14. Millman KJ
    15. Mayorov N
    16. Nelson ARJ
    17. Jones E
    18. Kern R
    19. Larson E
    20. Carey CJ
    21. Polat İ
    22. Feng Y
    23. Moore EW
    24. VanderPlas J
    25. Laxalde D
    26. Perktold J
    27. Cimrman R
    28. Henriksen I
    29. Quintero EA
    30. Harris CR
    31. Archibald AM
    32. Ribeiro AH
    33. Pedregosa F
    34. van Mulbregt P
    35. SciPy 1.0 Contributors

    (2020) SciPy 1.0: fundamental algorithms for scientific computing in python

    Nature Methods 17:261–272.

    https://doi.org/10.1038/s41592-019-0686-2

    • PubMed
    • Google Scholar
64. 1. Xu S
    2. Jiang W
    3. Poo MM
    4. Dan Y

    (2012) Activity recall in a visual cortical ensemble

    Nature Neuroscience 15:449–455.

    https://doi.org/10.1038/nn.3036

    • PubMed
    • Google Scholar

Author details

1. Matthias Ekman

   Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, Netherlands

   Contribution

   Conceptualization, Resources, Data curation, Software, Formal analysis, Supervision, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing

   For correspondence

   matthias.ekman@donders.ru.nl

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1254-1392

2. Sarah Kusch

   Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, Netherlands

   Contribution

   Conceptualization, Formal analysis, Methodology, Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

3. Floris P de Lange

   Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, Nijmegen, Netherlands

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Writing - review and editing

   Competing interests

   Senior editor, eLife

   "This ORCID iD identifies the author of this article:" 0000-0002-6730-1452

• 1,978

  Page views

• 203

  Downloads

• 8

  Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.