Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior

Hyman, James M.; Zilli, Eric A.; Paley, Amanda M.; Hasselmo, Michael E.

doi:10.1002/hipo.20106

Cited by 271 publications

(276 citation statements)

References 39 publications

(42 reference statements)

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“…These data are consistent with previous examinations of communication between the medial prefrontal cortex and hippocampus of rodents (Siapas et al, 2005;Wilson, 2005a, 2005b;Hyman et al, 2005Hyman et al, , 2010Sirota et al, 2008;Hartwich et al, 2009;Young and McNaughton, 2009;Adhikari et al, 2010;Benchenane et al, 2010; also reviewed by Colgin, 2011). Most research in this area has looked at neural activity correlations between the dorsal hippocampus and the prelimbic cortex, located just dorsal to the IL, and patterns have been linked to cognitive variables such as working memory (Jones and Wilson, 2005b;Hyman et al, 2005) and expectation-based decision-making (Benchenane et al, 2010). Meanwhile, coherence between the VH and the prelimbic cortex has been linked to anxiety (Adhikari et al, 2010).…”

Section: Discussionsupporting

confidence: 92%

Chronic deep brain stimulation of the rat ventral medial prefrontal cortex disrupts hippocampal–prefrontal coherence

Insel

Pilkiw

Nóbrega

et al. 2015

Experimental Neurology

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Deep brain stimulation (DBS) of the subgenual cingulate gyrus (SCG) has been used to treat patients with treatment-resistant depression. As in humans, DBS applied to the ventromedial prefrontal cortex of rats induces antidepressant-like responses. Physiological interactions between structures that play a role in depression and antidepressant treatment are still unknown. The present study examined the effect of DBS on inter-region communication by measuring the coherence of local field potentials in the rat infralimbic cortex (IL; homologue of the SCG) and one of its major afferents, the ventral hippocampus (VH). Rats received daily IL DBS treatment (100 μA, 90 μs, 130 Hz; 8 h/day). Recordings were conducted in unrestrained, behaving animals on the day before treatment, after 1 and 10 days of treatment, and 10 days stimulation offset. VH-IL coherence in the 2-4 Hz range was reduced in DBS-treated animals compared with shams after 10 days, but not after only 1 day of treatment. No effect of DBS was observed in the 6-10 Hz (theta) range, where coherence was generally high and could be further evoked with a loud auditory stimulus. Finally, coherence was not affected by fluoxetine (10 mg/kg), suggesting that the effects of DBS were not likely mediated by increased serotonin levels. While these data support the hypothesis that DBS disrupts communication between regions important for expectation-based control of emotion, they also suggest that lasting physiological effects require many days of treatment and, furthermore, may be specific to lower-frequency patterns, the nature and scope of which await further investigation.☆ NI, MP and CH designed the experiments; NI and MP performed the experiments; NI analyzed the data; NI, JN, WDH, KT, and CH wrote the paper.

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Section: Discussionsupporting

confidence: 92%

Chronic deep brain stimulation of the rat ventral medial prefrontal cortex disrupts hippocampal–prefrontal coherence

Insel

Pilkiw

Nóbrega

et al. 2015

Experimental Neurology

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“…Consistent with this view, PFC neurons exhibit context-dependent anticipatory neural codes for reward information (Pratt and Mizumori, 2001). Also, PFC neural signaling has been found to be conditionally linked to hippocampal output since PFC cell firing can become phase locked to CA1 hippocampal theta rhythms and precession (Hyman et al, 2005;Jones and Wilson, 2005). The entrained PFC neurons tended to be ones whose firing is correlated with specific behavioral acts (Hyman et al, 2005).…”

Section: Retrosplenial (Parietal) Cortex-hippocampal Interactionsmentioning

confidence: 81%

“…Also, PFC neural signaling has been found to be conditionally linked to hippocampal output since PFC cell firing can become phase locked to CA1 hippocampal theta rhythms and precession (Hyman et al, 2005;Jones and Wilson, 2005). The entrained PFC neurons tended to be ones whose firing is correlated with specific behavioral acts (Hyman et al, 2005). Furthermore, Hyman et al showed that testing subjects in different rooms caused some PFC neurons to change the degree to which they were entrained to the hippocampal theta rhythm, suggesting that the degree to which PFC is functionally connected to HPC was dependent on the stability of spatial context information…”

Section: Retrosplenial (Parietal) Cortex-hippocampal Interactionsmentioning

confidence: 99%

Hippocampal and neocortical interactions during context discrimination: Electrophysiological evidence from the rat

2007

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ABSTRACT:There is substantial evidence that hippocampus plays an important role in the processing of contextual information. Its specific role, however, remains unclear. One possibility is that single hippocampal neurons represent context information so that local circuits can construct representations of the current context, and the context that is expected based on past experience. Population codes derived from input by multiple local circuits may then engage match-mismatch algorithms that compare current and expected context information to determine the extent to which an expected context has changed. The results of such match-mismatch comparisons can be used to discriminate contexts. When context changes are detected, efferent messages may be passed on to connected neocortical areas so that informed "decisions" regarding future behavioral and cognitive strategies can be made. Here, a brief review describes evidence that a primary consequence of hippocampal processing is the discrimination of meaningful contexts. Then, the functional significance of neocortical circuits that likely receive hippocampal output messages are described in terms of their contribution to the control of ongoing behavioral and cognitive strategy, especially during active navigation. It is clear from this systems view that studies of spatial navigation continue to provide researchers with an excellent model of hippocampal-neocortical interactions during learning. V V C 2007 Wiley-Liss, Inc.

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“…Additionally, hippocampal theta may be important for organizing interactions between disparate brain regions. Neurons in multiple brain regions, including prefrontal cortex, are phase-locked to the hippocampal theta rhythm (54)(55)(56), and the amplitude of locally generated gamma-band (30-140 Hz) oscillations is also modulated by hippocampal theta phase (55,57,58). This latter phenomenon may be particularly important for memory, because gamma synchrony within and between MTL regions is enhanced during successful memory task performance (18,59,60).…”

Section: Discussionmentioning

confidence: 99%

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Jutras¹,

Fries

Buffalo

2013

Proc. Natl. Acad. Sci. U.S.A.

246

266

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Primates explore the visual world through the use of saccadic eye movements. Neuronal activity in the hippocampus, a structure known to be essential for memory, is modulated by this saccadic activity, but the relationship between visual exploration through saccades and memory formation is not well understood. Here, we identify a link between theta-band (3-12 Hz) oscillatory activity in the hippocampus and saccadic activity in monkeys performing a recognition memory task. As monkeys freely explored novel images, saccades produced a theta-band phase reset, and the reliability of this phase reset was predictive of subsequent recognition. In addition, enhanced theta-band power before stimulus onset predicted stronger stimulus encoding. Together, these data suggest that hippocampal theta-band oscillations act in concert with active exploration in the primate and possibly serve to establish the optimal conditions for stimulus encoding.T he use of saccadic eye movements to acquire information about the surrounding environment is perhaps the most conspicuous example of exploratory behavior in the primate. This behavior provides a mechanism for parsing incoming information into discrete, stable segments (i.e., snapshots of individual elements comprising a complex visual scene, allowing time for sufficient processing to occur before moving to the next fixation target). This mechanism of actively sampling sensory information from the environment may be similar to the behaviors engaged in by rodents exploring their environment through such activities as sniffing and whisking. Specifically, the fixation period following each saccade may be homologous to the period of incoming sensory information accompanying each sniff cycle in the rodent (1). Recently, it has been suggested that motor behaviors associated with information gathering are integral to the "active sensing" process in natural behavior (2). It is plausible that there may exist certain common neuronal elements across species that are associated with active sensing processes, such that the neuronal mechanisms underlying the encoding of information are intimately connected with the motor activities involved in acquiring that information.In many mammalian species, voluntary, exploratory behaviors are often associated with theta-band activity, a prominent 3-to 12-Hz oscillatory activity in the hippocampus and other limbic structures. This activity has been studied extensively in the rodent hippocampus (3-5), but it has also been described in bats (6), cats (7), and, more recently, humans (8-11). In rodents, theta appears to show close temporal relationships with running (3, 12) and sniffing (13), suggesting an association between theta and the rate of sensory input. Although hippocampal theta has been identified in anesthetized monkeys (14), the lack of a clear demonstration of hippocampal theta in awake monkeys has been attributed to the fact that the recording methods typically require immobile, head-affixed monkeys, in contrast to rodent studies using freely moving ...

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Medial prefrontal cortex cells show dynamic modulation with the hippocampal theta rhythm dependent on behavior

Cited by 271 publications

References 39 publications

Chronic deep brain stimulation of the rat ventral medial prefrontal cortex disrupts hippocampal–prefrontal coherence

Chronic deep brain stimulation of the rat ventral medial prefrontal cortex disrupts hippocampal–prefrontal coherence

Hippocampal and neocortical interactions during context discrimination: Electrophysiological evidence from the rat

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

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