Coupled Oscillations Mediate Directed Interactions between Prefrontal Cortex and Hippocampus of the Neonatal Rat

Brockmann, Marco D.; Poschel, B. P. H.; Cichon, Nicole; Hanganu‐Opatz, Ileana L.

doi:10.1016/j.neuron.2011.05.041

Cited by 174 publications

(341 citation statements)

References 59 publications

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“…Pregnant Wistar rats were obtained at 14 -17 d of gestation from the animal facility of the University Medical Center Hamburg-Eppendorf, housed individually in breeding cages with a 12 h light/dark cycle, and fed ad libitum. Extracellular recordings were performed in the PFC (2-2.5 mm anterior to bregma and 0.2-0.7 mm from the midline) and intermediate Hipp (3-4 mm posterior to bregma and 3-4 mm from the midline) of postnatal day 0 (P0) to P14 male rats (Ashwell and Paxinos at al., 2008) using experimental protocols as described previously Yang et al, 2009;Brockmann et al, 2011). Briefly, under light urethane anesthesia (0.5-1 g/kg; Sigma-Aldrich), the head of the pup was mounted into the stereotaxic apparatus (Stoelting) using two metal bars set in place with dental cement on the nasal and occipital bones, respectively.…”

Section: Methodsmentioning

confidence: 99%

“…Fast events (gamma episodes in the PFC, gamma oscillations and ripples in the Hipp) superimposed on slow events were detected either automatically or by eye and confirmed by time-frequency plots. Spindle bursts (SB) and nested gamma spindle bursts (NG) were classified according to previously described criteria (Khazipov et al, 2004;Brockmann et al, 2011). The presence of short gamma episodes automatically detected after 30 -100 Hz filtering and confirmed by eye on at least onethird of the cycles in intermittent slow oscillations led to classification of these events as NG.…”

Section: Methodsmentioning

confidence: 99%

“…We showed recently that hippocampal theta bursts drive the discontinuous activity of the neonatal PFC, whereas theta-gamma rhythms entrain the prejuvenile prefrontal-hippocampal networks (Brockmann et al, 2011). Here, we combined in vivo recordings from the neonatal and prejuvenile PFC and Hipp with pharmacological and immunohistochemical investigation as well as immunotoxic lesion.…”

Section: Introductionmentioning

confidence: 99%

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Cholinergic Control in Developing Prefrontal–Hippocampal Networks

Janiesch¹,

Krüger²,

Poschel³

et al. 2011

J. Neurosci.

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The cholinergic drive enhances input processing in attentional and mnemonic context by interacting with the activity of prefrontalhippocampal networks. During development, acetylcholine modulates neuronal proliferation, differentiation, and synaptic plasticity, yet its contribution to the maturation of cognitive processing resulting from early entrainment of neuronal networks in oscillatory rhythms remains widely unknown. Here we show that cholinergic projections growing into the rat prefrontal cortex (PFC) toward the end of the first postnatal week boost the generation of nested gamma oscillations superimposed on discontinuous spindle bursts by acting on functional muscarinic but not nicotinic receptors. Although electrical stimulation of cholinergic nuclei increased the occurrence of nested gamma spindle bursts by 41%, diminishment of the cholinergic input by either blockade of the receptors or chronic immunotoxic lesion had the opposite effect. This activation of locally generated gamma episodes by direct cholinergic projections to the PFC was accompanied by indirect modulation of underlying spindle bursts via cholinergic control of hippocampal theta activity. With ongoing maturation and switch of network activity from discontinuous bursts to continuous theta-gamma rhythms, accumulating cholinergic projections acting on both muscarinic and nicotinic receptors mediated the transition from high-amplitude slow to low-amplitude fast rhythms in the PFC. By exerting multiple actions on the oscillatory entrainment of developing prefrontal-hippocampal networks, the cholinergic input may refine them for later gating processing in executive and mnemonic tasks.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cholinergic Control in Developing Prefrontal–Hippocampal Networks

Janiesch¹,

Krüger²,

Poschel³

et al. 2011

J. Neurosci.

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show abstract

“…Previously, this type of plasticity was reported in the developing PFC, which facilitates the morphological and functional changes necessary to refine behaviorally relevant communication derived from hippocampal oscillatory activity (Brockmann et al, 2011). Although gene expression studies have been reported for neonatal marmoset hippocampus using marmoset-specific DNA microarray (Datson et al, 2009), we examined molecules whose expression has not been reported in wider regions such as the entorhinal (Ent) cortex.…”

Section: Dynamic Gene Expression In Efferent Regions Of the Pfc-hippomentioning

confidence: 98%

Comparative Anatomy of Marmoset and Mouse Cortex from Genomic Expression

et al. 2012

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Advances in mouse neural circuit genetics, brain atlases, and behavioral assays provide a powerful system for modeling the genetic basis of cognition and psychiatric disease. However, a critical limitation of this approach is how to achieve concordance of mouse neurobiology with the ultimate goal of understanding the human brain. Previously, the common marmoset has shown promise as a genetic model system toward the linking of mouse and human studies. However, the advent of marmoset transgenic approaches will require an understanding of developmental principles in marmoset compared to mouse. In this study, we used gene expression analysis in marmoset brain to pose a series of fundamental questions on cortical development and evolution for direct comparison to existing mouse brain atlas expression data. Most genes showed reliable conservation of expression between marmoset and mouse. However, certain markers had strikingly divergent expression patterns. The lateral geniculate nucleus and pulvinar in the thalamus showed diversification of genetic organization between marmoset and mouse, suggesting they share some similarity. In contrast, gene expression patterns in early visual cortical areas showed marmoset-specific expression. In prefrontal cortex, some markers labeled architectonic areas and layers distinct between mouse and marmoset. Core hippocampus was conserved, while afferent areas showed divergence. Together, these results indicate that existing cortical areas are genetically conserved between marmoset and mouse, while differences in areal parcellation, afferent diversification, and layer complexity are associated with specific genes. Collectively, we propose that gene expression patterns in marmoset brain reveal important clues to the principles underlying the molecular evolution of cortical and cognitive expansion.

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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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Coupled Oscillations Mediate Directed Interactions between Prefrontal Cortex and Hippocampus of the Neonatal Rat

Cited by 174 publications

References 59 publications

Cholinergic Control in Developing Prefrontal–Hippocampal Networks

Cholinergic Control in Developing Prefrontal–Hippocampal Networks

Comparative Anatomy of Marmoset and Mouse Cortex from Genomic Expression

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

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