Interactive effects of stress reactivity and rapid eye movement sleep theta activity on emotional memory formation

Sleep and stress independently enhance emotional memory consolidation. In particular, theta oscillations (4–7 Hz) during rapid eye movement (REM) sleep increase coherence in an emotional memory network (i.e., hippocampus, amygdala, and prefrontal cortex) and enhance emotional memory. However, little is known about how stress during learning might interact with subsequent REM theta activity to affect emotional memory. In the current study, we examined whether the relationship between REM theta activity and emotional memory differs as a function of pre‐encoding stress exposure and reactivity. Participants underwent a psychosocial stressor (the Trier Social Stress Task; n = 32) or a comparable control task (n = 32) prior to encoding. Task‐evoked cortisol reactivity was assessed by salivary cortisol rise from pre‐ to post‐stressor, and participants in the stress condition were additionally categorized as high or low cortisol responders via a median split. During incidental encoding, participants studied 150 line drawings of negative, neutral, and positive images, followed by the complete color photo. All participants then slept overnight in the lab with polysomnographic recording. The next day, they were given a surprise recognition memory task. Results showed that memory was better for emotional relative to neutral information. Critically, these findings were observed only in the stress condition. No emotional memory benefit was observed in the control condition. In stressed participants, REM theta power significantly predicted memory for emotional information, specifically for positive items. This relationship was observed only in high cortisol responders. For low responders and controls, there was no relationship between REM theta and memory of any valence. These findings provide evidence that elevated stress at encoding, and accompanying changes in neuromodulators such as cortisol, may interact with theta activity during REM sleep to promote selective consolidation of emotional information.     

Hippocampal Theta Oscillations Support Successful Associative Memory Formation

Models of memory formation posit that episodic memory formation depends critically on the hippocampus, which binds features of an event to its context. For this reason, the contrast between study items that are later recollected with their associative pair versus those for which no association is made fails should reveal electrophysiological patterns in the hippocampus selectively involved in associative memory encoding. Extensive data from studies in rodents support a model in which theta oscillations fulfill this role, but results in humans have not been as clear. Here, we used an associative recognition memory procedure to identify hippocampal correlates of successful associative memory encoding and retrieval in patients (10 females and 9 males) undergoing intracranial EEG monitoring. We identified a dissociation between 2–5 Hz and 5–9 Hz theta oscillations, by which power increases in 2–5 Hz oscillations were uniquely linked with successful associative memory in both the anterior and posterior hippocampus. These oscillations exhibited a significant phase reset that also predicted successful associative encoding and distinguished recollected from nonrecollected items at retrieval, as well as contributing to relatively greater reinstatement of encoding-related patterns for recollected versus nonrecollected items. Our results provide direct electrophysiological evidence that 2–5 Hz hippocampal theta oscillations preferentially support the formation of associative memories, although we also observed memory-related effects in the 5–9 Hz frequency range using measures such as phase reset and reinstatement of oscillatory activity.SIGNIFICANCE STATEMENT Models of episodic memory encoding predict that theta oscillations support the formation of interitem associations. We used an associative recognition task designed to elicit strong hippocampal activation to test this prediction in human neurosurgical patients implanted with intracranial electrodes. The findings suggest that 2–5 Hz theta oscillatory power and phase reset in the hippocampus are selectively associated with associative memory judgments. Furthermore, reinstatement of oscillatory patterns in the hippocampus was stronger for successful recollection. Collectively, the findings support a role for hippocampal theta oscillations in human associative memory.     

The functional role of human right hippocampal/parahippocampal theta rhythm in environmental encoding during virtual spatial navigation

Low frequency theta band oscillations (4–8 Hz) are thought to provide a timing mechanism for hippocampal place cell firing and to mediate the formation of spatial memory. In rodents, hippocampal theta has been shown to play an important role in encoding a new environment during spatial navigation, but a similar functional role of hippocampal theta in humans has not been firmly established. To investigate this question, we recorded healthy participants’ brain responses with a 160‐channel whole‐head MEG system as they performed two training sets of a virtual Morris water maze task. Environment layouts (except for platform locations) of the two sets were kept constant to measure theta activity during spatial learning in new and familiar environments. In line with previous findings, left hippocampal/parahippocampal theta showed more activation navigating to a hidden platform relative to random swimming. Consistent with our hypothesis, right hippocampal/parahippocampal theta was stronger during the first training set compared to the second one. Notably, theta in this region during the first training set correlated with spatial navigation performance across individuals in both training sets. These results strongly argue for the functional importance of right hippocampal theta in initial encoding of configural properties of an environment during spatial navigation. Our findings provide important evidence that right hippocampal/parahippocampal theta activity is associated with environmental encoding in the human brain. Hum Brain Mapp 38:1347–1361, 2017. © 2016 Wiley Periodicals, Inc.     

Different brain activities predict retrieval success during emotional and semantic encoding

There is an increasing line of evidence supporting the idea that the formation of lasting memories involves neural activity preceding stimulus presentation. Following this line, we presented words in an incidental learning setting and manipulated the prestimulus state by asking the participants to perform either an emotional (neutral or emotional) or a semantic (animate or inanimate) decision task. Later, we tested the retrieval of each previously presented word with a recognition memory test. For both conditions, the subsequent memory effect (SME) was defined as ERP difference between subsequently remembered and forgotten words. Comparing the prestimulus SME between and within the two conditions yielded topographic differences in the time interval from -1300 to -700 msec before stimulus onset. This indicates that the activity of brain areas involved in incidental encoding of semantic information varied in the spatial distribution of ERPs, depending on the emotional and semantic requirements of the task. These findings provide evidence that there is a difference in semantic and emotional preparatory processes, which modulates successful encoding into episodic memory. This difference suggests that there are multiple task-specific functional neural systems that support memory formation. These systems differ in location and/or relative contribution of some of the brain structures that generate the measured scalp electric fields. Consequently, the cognitive processes that enable memory formation depend on the differential semantic nature of the study task and reflect differences in the preparatory processing of the multiple semantic components of a word's meaning.     

Medial Prefrontal Cortex Has a Causal Role in Selectively Enhanced Consolidation of Emotional Memories after a 24-Hour Delay: A TBS Study

Previous research points to an association between retrieval-related activity in the medial prefrontal cortex (mPFC) and preservation of emotional information compared with co-occurring neutral information following sleep. Although the role of the mPFC in emotional memory likely begins at encoding, little research has examined how mPFC activity during encoding interacts with consolidation processes to enhance emotional memory. This issue was addressed in the present study using transcranial magnetic stimulation in conjunction with an emotional memory paradigm. Healthy young adults encoded negative and neutral scenes while undergoing concurrent TMS with a modified short intermittent theta burst stimulation (sTBS) protocol. Participants received stimulation to either the mPFC or an active control site (motor cortex) during the encoding phase. Recognition memory for scene components (objects and backgrounds) was assessed after a short delay (30 min) and a long delay [24 h (including a night of sleep)] to obtain measures of specific and gist-based memory processes. The results demonstrated that, relative to control stimulation, sTBS to the mPFC enhanced memory for negative objects on the long delay test (collapsed across specific and gist-based memory measures). mPFC stimulation had no discernable effect on memory for objects on the short delay test nor on the background images at either test. These results suggest that mPFC activity occurring during encoding interacts with consolidation processes to preferentially preserve negatively salient information.SIGNIFICANCE STATEMENT Understanding how emotional information is remembered over time is critical to understanding memory in the real world. The present study used noninvasive brain stimulation [repetitive transcranial magnetic stimulation (rTMS)] to investigate the interplay between mPFC activity that occurs during memory encoding and its subsequent interactions with consolidation processes. rTMS delivered to the mPFC during encoding enhanced memory for negatively valenced pictures on a test following a 24 h delay, with no such effect on a test occurring shortly after the encoding phase. These results are consistent with the hypothesis that emotional aspects of memories are differentially subjected to consolidation processes, and that the mPFC might contribute to this “tag-and-capture” mechanism during the initial formation of such memories.     

Phase-locked alpha and theta oscillations generate the P1-N1 complex and are related to memory performance

An oscillatory phase resetting model is presented and data are reported which indicate that early components of the event-related potential are due to the superposition of evoked oscillations. The following hypotheses were tested and could be confirmed: (i) theta and alpha show a significant increase in phase locking during the time window of the P1 and N1 as compared to a prestimulus reference, (ii) the dynamics of event-related changes in evoked theta and alpha power obey the same principles as are known from event-related de-/synchronization research, and (iii) latency measures of the P1-N1 complex are negatively correlated with individual alpha frequency. In addition, we have found that theta phase locking is larger during encoding than recognition and that good memory performers show a larger increase in theta and alpha phase locking during recognition in the time window of the N1. Our general conclusion is that the P1-N1 complex is generated primarily by evoked alpha and theta oscillations reflecting the synchronous activation of a working- and semantic memory system.     

Induced electroencephalogram oscillations during source memory: familiarity is reflected in the gamma band, recollection in the theta band

Modulations of oscillatory electroencephalogram (EEG) activity in the induced gamma and theta frequency ranges (induced gamma and theta band responses; iGBRs: >30 Hz; iTBRs: approximately 6 Hz) have been associated with retrieval of information from long-term memory. However, the specific functional role of these two forms of oscillatory activity remains unclear. The present study examines theta- and gamma-oscillations within a dual-process framework, which defines "familiarity" and "recollection" as the two component processes of recognition memory. During encoding, participants were instructed to make "bigger/smaller than a shoebox" or "living/nonliving" decisions for different object pictures. During retrieval "old/new" recognition was followed (for items judged old) by a source discrimination task regarding the decision made for each item at encoding. iGBRs (35-80 Hz; 210-330 msec) were higher for correctly identified "old" relative to "new" objects. Importantly, they did not distinguish between successful and unsuccessful source judgments. In contrast, iTBRs (4-7.5 Hz; 600-1200 msec) were sensitive to source discrimination. We propose that iGBRs mirror early associative processes linked to familiarity-related retrieval processes, whereas iTBRs reflect later onsetting, episodic, recollection-related mechanisms.     

Event-induced theta responses as a window on the dynamics of memory

An important, but often ignored distinction in the analysis of EEG signals is that between evoked activity and induced activity. Whereas evoked activity reflects the summation of transient post-synaptic potentials triggered by an event, induced activity, which is mainly oscillatory in nature, is thought to reflect changes in parameters controlling dynamic interactions within and between brain structures. We hypothesize that induced activity may yield information about the dynamics of cell assembly formation, activation and subsequent uncoupling, which may play a prominent role in different types of memory operations. We then describe a number of analysis tools that can be used to study the reactivity of induced rhythmic activity, both in terms of amplitude changes and of phase variability.

We briefly discuss how alpha, gamma and theta rhythms are thought to be generated, paying special attention to the hypothesis that the theta rhythm reflects dynamic interactions between the hippocampal system and the neocortex. This hypothesis would imply that studying the reactivity of scalp-recorded theta may provide a window on the contribution of the hippocampus to memory functions.

We review studies investigating the reactivity of scalp-recorded theta in paradigms engaging episodic memory, spatial memory and working memory. In addition, we review studies that relate theta reactivity to processes at the interface of memory and language. Despite many unknowns, the experimental evidence largely supports the hypothesis that theta activity plays a functional role in cell assembly formation, a process which may constitute the neural basis of memory formation and retrieval. The available data provide only highly indirect support for the hypothesis that scalp-recorded theta yields information about hippocampal functioning. It is concluded that studying induced rhythmic activity holds promise as an additional important way to study brain function.     

Encoding of rat working memory by power of multi-channel local field potentials via sparse non-negative matrix factorization

Working memory plays an important role in human cognition. This study investigated how working memory was encoded by the power of multi-channel local field potentials (LFPs) based on sparse nonnegative matrix factorization (SNMF). SNMF was used to extract features from LFPs recorded from the prefrontal cortex of four Sprague-Dawley rats during a memory task in a Y maze, with 10 trials for each rat. Then the power-increased LFP components were selected as working memory-related features and the other components were removed. After that, the inverse operation of SNMF was used to study the encoding of working memory in the time-frequency domain. We demonstrated that theta and gamma power increased significantly during the working memory task. The results suggested that postsynaptic activity was simulated well by the sparse activity model. The theta and gamma bands were meaningful for encoding working memory.     

Cosine directional tuning of theta cell burst frequencies: evidence for spatial coding by oscillatory interference

The rodent septohippocampal system contains "theta cells," which burst rhythmically at 4-12 Hz, but the functional significance of this rhythm remains poorly understood (Buzsáki, 2006). Theta rhythm commonly modulates the spike trains of spatially tuned neurons such as place (O'Keefe and Dostrovsky, 1971), head direction (Tsanov et al., 2011a), grid (Hafting et al., 2005), and border cells (Savelli et al., 2008; Solstad et al., 2008). An "oscillatory interference" theory has hypothesized that some of these spatially tuned neurons may derive their positional firing from phase interference among theta oscillations with frequencies that are modulated by the speed and direction of translational movements (Burgess et al., 2005, 2007). This theory is supported by studies reporting modulation of theta frequency by movement speed (Rivas et al., 1996; Geisler et al., 2007; Jeewajee et al., 2008a), but modulation of theta frequency by movement direction has never been observed. Here we recorded theta cells from hippocampus, medial septum, and anterior thalamus of freely behaving rats. Theta cell burst frequencies varied as the cosine of the rat's movement direction, and this directional tuning was influenced by landmark cues, in agreement with predictions of the oscillatory interference theory. Computer simulations and mathematical analysis demonstrated how a postsynaptic neuron can detect location-dependent synchrony among inputs from such theta cells, and thereby mimic the spatial tuning properties of place, grid, or border cells. These results suggest that theta cells may serve a high-level computational function by encoding a basis set of oscillatory signals that interfere with one another to synthesize spatial memory representations.     

Spatiotemporal and spectral dynamics of multi‐item working memory as revealed by the n‐back task using MEG

Multi‐item working memory (WM) is a complex cognitive function thought to arise from specific frequency band oscillations and their interactions. While some theories and consistent findings have been established, there is still a lot of unclarity about the sources, temporal dynamics, and roles of event‐related fields (ERFs) and theta, alpha, and beta oscillations during WM activity. In this study, we performed an extensive whole‐brain ERF and time‐frequency analysis on n‐back magnetoencephalography data from 38 healthy controls. We identified the previously unknown sources of the n‐back M300, the right inferior temporal and parahippocampal gyrus and left inferior temporal gyrus, and frontal theta power increase, the orbitofrontal cortex. We shed new light on the role of the precuneus during n‐back activity, based on an early ERF and theta power increase, and suggest it to be a crucial link between lower‐level and higher‐level information processing. In addition, we provide strong evidence for the central role of the hippocampus in multi‐item WM behavior through the dynamics of theta and alpha oscillatory changes. Almost simultaneous alpha power decreases observed in the hippocampus and occipital fusiform gyri, regions known to be involved in letter processing, suggest that these regions together enable letter recognition, encoding and storage in WM. In summary, this study offers an extensive investigation into the spatial, temporal, and spectral characteristics of n‐back multi‐item WM activity.     

The relationship between brain oscillations and BOLD signal during memory formation: a combined EEG-fMRI study

Previous studies demonstrated that increases in the theta frequency band with concomitant decreases in the alpha/beta frequency band indicate successful memory formation. However, little is known about the brain regions and the cognitive processes that underlie these encoding-related oscillatory memory effects. We investigated this relationship using simultaneous EEG-fMRI recordings in humans during long-term memory encoding. In line with prior studies, we demonstrate that a decrease in beta power and an increase in theta power positively predict subsequent recall. In fMRI, stronger activity in the left inferior prefrontal cortex and the right parahippocampal gyrus correlated with successful memory formation. EEG source localization revealed that the subsequent memory effect in the beta band was localized in the left inferior prefrontal cortex, whereas the effect in the theta band was localized in medial temporal lobe regions. Trial-by-trial correlations between EEG and BOLD activity showed that beta power correlated negatively with left inferior prefrontal cortex activity. This correlation was more pronounced for items that could later be successfully recalled compared to items later forgotten. Based on these findings, we suggest that beta oscillations in the left inferior prefrontal cortex indicate semantic encoding processes, whereas theta oscillations in the medial temporal lobe reflect the binding of an item to its spatiotemporal context.     

Frontal theta event-related synchronization: comparison of directed attention and working memory load effects

Summary. Early studies showed that long-term encoding and retrieval of new information is associated with modulation of the theta rhythm. More recently, changes in theta power amplitude over frontal electrode sites were reported during working memory, yet their relative significance in regard to attentional and memory processes remains unclear. Event-related synchronisation responses in the 4–7.5 Hz theta EEG frequency band was studied in 12 normal subjects performing four different tasks: two working memory tasks in which load varied from one (1-back task) to two (2-back task) items, an oddball detection (attention) task and a passive fixation task. A phasic theta increase was observed following stimulus apparition on all electrode sites within each task, with longer culmination peak and maximal amplitude over frontal electrodes. Frontal theta event-related synchronization (ERS) was of higher amplitude in the 1-back, 2-back and detection tasks as compared to the passive fixation task. Additionally, the detection task elicited a larger frontal and central theta ERS than the 2-back task. By analyzing theta ERS characteristics in various experimental conditions, the present study reveals that early phasic theta response over frontal regions primarily reflects the activation of neural networks involved in allocation of attention related to target stimuli rather than working memory processes.     

Behavioral anxiolysis without reduction of hippocampal theta frequency after histamine application in the lateral septum of rats

Hippocampal theta activity is linked to various processes, including locomotion, learning and memory, and defense and affect (i.e., fear and anxiety). Interestingly, all classes of clinically effective anxiolytics, as well as experimental compounds that decrease anxiety in pre‐clinical animal models of anxiety, reduce the frequency of hippocampal theta activity elicited by stimulation of the reticular formation in freely behaving or anesthetized animals. In the present experiments, we found that bilateral histamine infusions (0.5 µg/hemisphere) into the lateral septum (LS) of rats decreased anxiety‐like responses in two models of anxiety, the elevated plus maze and novelty‐induced suppression of feeding test. Surprisingly, these same infusions significantly increased hippocampal theta frequency elicited by reticular stimulation in urethane‐anesthetized rats. In contrast to these findings, additional experiments showed that the clinically effective anxiolytic buspirone (40 mg/kg, i.p.) reduced theta frequency, confirming previous observations. Taken together, the dissociation of behavioral anxiolysis and theta frequency reduction noted here suggest that hippocampal theta frequency is not a direct index of anxiety levels in rodents. Further, the mechanisms underlying the behavioral and physiological effects elicited by histamine in the LS require further study. © 2014 Wiley Periodicals, Inc.     

Model-driven neuromodulation of the right posterior region promotes encoding of long-term memories

BackgroundLong-term recognition memory depends both on initial encoding and on subsequent recognition processes.ObjectiveIn this study we aimed at improving long-term memory by modulating posterior parietal brain activity during the encoding process. If this area is causally involved in memory encoding, its facilitation should lead to behavioral improvement. Based on the dual-process memory framework, we also expected that the neuromodulation would dissociate subsequent familiarity-based and recollection-based recognition.MethodsWe investigated the role of the posterior parietal brain oscillations in facial memory formation in three separate experiments using electroencephalography (EEG), functional magnetic resonance imaging (fMRI), and model-driven, multi-electrode transcranial alternating current stimulation (tACS).ResultsUsing fMRI and EEG, we confirmed that the right posterior parietal cortex is an essential node that promotes the encoding of long-term memories. We found that single-trial low theta power in this region predicts subsequent long-term recognition. On this basis, we fine-tuned the spatial and frequency settings of tACS during memory encoding. Model-driven tACS over the right posterior brain area augmented subsequent long-term recognition memory and particularly the familiarity of the observed stimuli. The recollection process, and short-term task performance as control remained unchanged. Control stimulation over the left hemisphere had no behavioral effect.ConclusionWe conclude that the right posterior brain area is crucial in long-term memory encoding.     

Top-down modulation of hippocampal encoding activity as measured by high-resolution functional MRI

Memory formation is known to be critically dependent upon the medial temporal lobe (MTL). Despite this well-characterized role, it remains unclear whether and how MTL encoding processes are affected by top-down goal states. Here, we examined the manner in which task demands at encoding affect MTL activity and its relation to subsequent memory performance. Participants were scanned using high-resolution neuroimaging of the MTL while engaging in two incidental encoding tasks: one that directed participants’ attention to stimulus distinctiveness, and the other requiring evaluation of similarities across stimuli. We hypothesized that attending to distinctiveness would lead to the formation of more detailed memories and would more effectively engage the hippocampal circuit than attending to similarity. In line with our hypotheses, higher rates of subsequent recollection were observed for stimuli studied under the Distinctiveness than Similarity task. Critically, within the hippocampus, CA1 and the subiculum demonstrated an interaction between memory performance and task such that a significant subsequent memory effect was found only when task goals required attention to stimulus distinctiveness. To this end, robust engagement of the hippocampal circuit may underlie the observed behavioral benefits of attending to distinctiveness. Taken together, these findings advance understanding of the effects of top-down intentional information on successful memory formation across subregions of the MTL.     

Perturbation of theta-gamma coupling at the temporal lobe hinders verbal declarative memory

Background

Phase-amplitude cross-frequency coupling (PAC) is characterized by the modulation of the power of a fast brain oscillation (e.g., gamma) by the phase of a slow rhythm (e.g., theta). PAC in different sub- and neocortical regions is known to underlie effective neural communication and correlates with successful long-term memory formation.

Is there “neural efficiency” during the processing of visuo-spatial information in male humans? An EEG study

More intelligent persons (high IQ) typically present a higher cortical activity during tasks requiring the encoding of visuo-spatial information, namely higher alpha (about 10 Hz) event-related desynchronization (ERD; Doppelmayr et al., 2005 [23]). The opposite is true (“neural efficiency”) during the retrieval of the encoded information, as revealed by both lower alpha ERD and/or lower theta (about 5 Hz) event-related synchronization (ERS; Grabner et al., 2004 [19]). To reconcile these contrasting results, here we evaluated the working hypothesis that more intelligent male subjects are characterized by a high cortical activity during the encoding phase. This deep encoding would explain the relatively low cortical activity for the retrieval of the encoded information. To test this hypothesis, electroencephalographic (EEG) data were recorded in 22 healthy young male volunteers during visuo-spatial information processing (encoding) and short-term retrieval of the encoded information. Cortical activity was indexed by theta ERS and alpha ERD. It was found that the higher the subjects’ total IQ, the stronger the frontal theta ERS during the encoding task. Furthermore, the higher the subjects’ total IQ, the lower the frontal high-frequency alpha ERD (about 10–12 Hz) during the retrieval task. This was not true for parietal counterpart of these EEG rhythms. These results reconcile previous contrasting evidence confirming that more intelligent persons do not ever show event-related cortical responses compatible with “neural efficiency” hypothesis. Rather, their cortical activity would depend on flexible and task-adapting features of frontal activation.     

The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme

In the hippocampus, oscillations in the theta and gamma frequency range occur together and interact in several ways, indicating that they are part of a common functional system. It is argued that these oscillations form a coding scheme that is used in the hippocampus to organize the readout from long-term memory of the discrete sequence of upcoming places, as cued by current position. This readout of place cells has been analyzed in several ways. First, plots of the theta phase of spikes vs. position on a track show a systematic progression of phase as rats run through a place field. This is termed the phase precession. Second, two cells with nearby place fields have a systematic difference in phase, as indicated by a cross-correlation having a peak with a temporal offset that is a significant fraction of a theta cycle. Third, several different decoding algorithms demonstrate the information content of theta phase in predicting the animal's position. It appears that small phase differences corresponding to jitter within a gamma cycle do not carry information. This evidence, together with the finding that principle cells fire preferentially at a given gamma phase, supports the concept of theta/gamma coding: a given place is encoded by the spatial pattern of neurons that fire in a given gamma cycle (the exact timing within a gamma cycle being unimportant); sequential places are encoded in sequential gamma subcycles of the theta cycle (i.e., with different discrete theta phase). It appears that this general form of coding is not restricted to readout of information from long-term memory in the hippocampus because similar patterns of theta/gamma oscillations have been observed in multiple brain regions, including regions involved in working memory and sensory integration. It is suggested that dual oscillations serve a general function: the encoding of multiple units of information (items) in a way that preserves their serial order. The relationship of such coding to that proposed by Singer and von der Malsburg is discussed; in their scheme, theta is not considered. It is argued that what theta provides is the absolute phase reference needed for encoding order. Theta/gamma coding therefore bears some relationship to the concept of "word" in digital computers, with word length corresponding to the number of gamma cycles within a theta cycle, and discrete phase corresponding to the ordered "place" within a word.     

Online formation of a hierarchical cognitive map for object-place association by theta phase coding

Object-place associative memory, the storage of object and place conjunctions based on a one-time experience, is hippocampal-dependent in humans. Theta phase precession, a type of neural dynamics observed in the rat hippocampus, has recently been suggested to serve a role in instantaneous memory formation based on a one-time experience, while its functional role in associating distinct types of information (object and place information) is unclear. In this study, we hypothesize that theta phase encoding with theta phase precession contributes to the storage of object-place associations. To examine this hypothesis, we propose a neural network model of the corticohippocampal system, including central-peripheral visual pathways and theta phase coding in the hippocampus. Memory storage computer experiments demonstrate that the hippocampal network successfully stores the object-place associations of a one-time experience. Interestingly, it is also found that a random visual input sequence results in a robust formation of asymmetric connections between objects and scenes instantaneously after a single trial. Furthermore, it is found that scene-object connections and scene-scene connections form a hierarchical network representing the spatial alignment of scenes and objects in the environment. Our findings indicate that the theta phase coding, as observed in the rat hippocampus, can facilitate the online memory storage of complex environments in humans as a hierarchical cognitive map.