Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates

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

doi:10.3389/neuro.07.002.2010

Cited by 182 publications

(253 citation statements)

References 55 publications

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“…VH-IL coherence in both treatment groups was strongest within the 6 to 10 Hz theta frequency band. 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).…”

Section: Discussionsupporting

confidence: 72%

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: 72%

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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“…3a) (Jones and Wilson, 2005;Benchenane et al, 2010;Hyman et al, 2010). Elevated hippocampal theta power evident throughout these choice runs was attenuated postdrug ( p ϭ 0.041; Fig.…”

Section: Network Oscillations During a Spatial Working Memory Taskmentioning

confidence: 98%

“…Behavior-dependent phase alignment to hippocampal theta also occurs in amygdala (Pape et al, 2005), dorsal and ventral striatum (Tort et al, 2008;van der Meer and Redish, 2011), and prefrontal cortex (Siapas et al, 2005), prompting the concept of a theta phase code transmitted via coordinated oscillations between hippocampus and functionally connected brain regions (Hasselmo, 2005;Jensen and Lisman, 2005). Hippocampal-prefrontal interactions in the theta frequency range have been consistently implicated in functions associated with working memory in rats and humans (Jones and Wilson, 2005;Anderson et al, 2010;Benchenane et al, 2010;Hyman et al, 2010) and provide a potential mechanism for integration of mnemonic and decision-making processes during goal-directed behaviors (Sauseng et al, 2010;Fell and Axmacher, 2011). Accordingly, aberrant oscillatory activity is associated with impaired cognition in a wide range of neuropsychiatric disorders (Uhlhaas and Singer, 2006) and may cause and/or reflect impaired limbic-cortical interactions in disease.…”

Section: Introductionmentioning

confidence: 99%

Dysfunctional Prefrontal Cortical Network Activity and Interactions following Cannabinoid Receptor Activation

Kucewicz¹,

Tricklebank²,

Bogacz³

et al. 2011

J. Neurosci.

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Coordinated activity spanning anatomically distributed neuronal networks underpins cognition and mediates limbic-cortical interactions during learning, memory, and decision-making. We used CP55940, a potent agonist of brain cannabinoid receptors known to disrupt coordinated activity in hippocampus, to investigate the roles of network oscillations during hippocampal and medial prefrontal cortical (mPFC) interactions in rats. During quiet wakefulness and rest, CP55940 dose-dependently reduced 0.1-30 Hz local field potential power in CA1 of the hippocampus while concurrently decreasing 30 -100 Hz power in mPFC; these contrasting population-level effects were paralleled by differential effects on underlying single-unit activity in the two structures. During decision-making phases of a spatial working memory task, CP5540-induced deficits in hippocampal theta and prefrontal gamma oscillations were observed alongside disrupted theta-frequency coherence between the two structures. These changes in coordinated limbic-cortical network activities correlated with (1) reduced accuracy of task performance, (2) impaired phase-locking of prefrontal single-unit spiking to the local gamma and hippocampal theta rhythms, and (3) impaired task-dependent activity in a subset of mPFC units. In addition to highlighting the importance of CA1-mPFC network oscillations for cognition, these results implicate disrupted theta-frequency coordination of CA1-mPFC activity in the cognitive deficits caused by exogenous activation of brain cannabinoid receptors.

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“…For example, numerous investigations of prefrontal and hippocampal circuits in both rodents and humans highlight the importance of theta (4-10 Hz) and gamma (32-150 Hz) rhythms and their interaction for the successful integration of both spatial and non-spatial information during goal-directed behaviors (Jones and Wilson, 2005;Sirota et al, 2008;Anderson et al, 2010;Benchenane et al, 2010;Hyman et al, 2010;Womelsdorf et al, 2010;Brockmann et al, 2011). These oscillatory rhythms emerge from interactions between excitatory glutamatergic and inhibitory GABAergic neurotransmission, which are in turn subject to behavior-dependent neuromodulation.…”

Section: Introductionmentioning

confidence: 99%

Losing Control Under Ketamine: Suppressed Cortico-Hippocampal Drive Following Acute Ketamine in Rats

Moran

Jones

Blockeel

et al. 2014

Neuropsychopharmacol

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Systemic doses of the psychotomimetic ketamine alter the spectral characteristics of hippocampal and prefrontal cortical network activity. Using dynamic causal modeling (DCM) of cross-spectral densities, we quantify the putative synaptic mechanisms underlying ketamine effects in terms of changes in directed, effective connectivity between dorsal hippocampus and medial prefrontal (dCA1-mPFC) cortex of freely moving rats. We parameterize dose-dependent changes in spectral signatures of dCA1-mPFC local field potential recordings, using neural mass models of glutamatergic and GABAergic circuits. Optimizing DCMs of theta and gamma frequency range responses, model comparisons suggest that both enhanced gamma and depressed theta power result from a reduction in top-down connectivity from mPFC to the hippocampus, mediated by postsynaptic NMDA receptors (NMDARs). This is accompanied by an alteration in the bottom-up pathway from dCA1 to mPFC, which exhibits a distinct asymmetry: here, feed-forward drive at AMPA receptors increases in the presence of decreased NMDAR-mediated inputs. Setting these findings in the context of predictive coding suggests that NMDAR antagonism by ketamine in recurrent hierarchical networks may result in the failure of top-down connections from higher cortical regions to signal predictions to lower regions in the hierarchy, which consequently fail to respond consistently to errors. Given that NMDAR dysfunction has a central role in pathophysiological theories of schizophrenia and that theta and gamma rhythm abnormalities are evident in schizophrenic patients, the approach followed here may furnish a framework for the study of aberrant hierarchical message passing (of prediction errors) in schizophrenia-and the false perceptual inferences that ensue.

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Working memory performance correlates with prefrontal-hippocampal theta interactions but not with prefrontal neuron firing rates

Cited by 182 publications

References 55 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

Dysfunctional Prefrontal Cortical Network Activity and Interactions following Cannabinoid Receptor Activation

Losing Control Under Ketamine: Suppressed Cortico-Hippocampal Drive Following Acute Ketamine in Rats

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