Membrane and circuit properties of lateral septum neurons: relationships with hippocampal rhythms

Pedemonte, Marisa; Barrenechea, Carmen; Núñez, Ángel; Gambini, Juan; García-Austt, E.

doi:10.1016/s0006-8993(98)00517-4

Cited by 36 publications

(37 citation statements)

References 36 publications

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“…Finally, the LS itself receives substantial glutamatergic input from the hippocampus (Risold and Swanson 1997), suggesting the possibility of a feed-forward mechanism to regulate theta activity. Indeed, it has been hypothesized that the LS modulates theta generation by using feedback from the hippocampus to regulate the firing of neurons in the MS (McLennon andMiller 1974, 1976;Pedemont et al 1998;Vinogradova 1995). This anatomical and neurochemical evidence, together with the results obtained in the present experiments, is consistent with the hypothesis that the LS, via its GABAergic projections to structures in the ascending theta generation pathway, normally exerts a profound, inhibitory influence on hippocampal theta activity.…”

Section: Discussionsupporting

confidence: 91%

“…As such, whether the increase in theta frequency following intra-LS application of histamine resulted from excitation or inhibition of the LS is unknown. Curiously, although the LS has been suggested to be an important mediator of the theta rhythm (Vinogradova 1995), few (e.g., McLennon andMiller 1974, 1976;Pedemont et al 1998) have investigated its precise role in modulating theta generation. Thus here we examined the effects of direct, pharmacological inhibition or disinhibition of dorsal LS (dLS) activity by local application of muscimol (GABA A receptor agonist) or GABAzine (GABA A receptor antagonist), respectively, on hippocampal theta frequency in urethane-anesthetized rats.…”

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confidence: 99%

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The lateral septum as a regulator of hippocampal theta oscillations and defensive behavior in rats

Chee

Menard

Dringenberg

2015

Journal of Neurophysiology

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Chee S-SA, Menard JL, Dringenberg HC. The lateral septum as a regulator of hippocampal theta oscillations and defensive behavior in rats. J Neurophysiol 113: 1831-1841, 2015. First published January 14, 2015 doi:10.1152/jn.00806.2014.-Hippocampal theta oscillations are linked to various processes, including locomotion, learning and memory, and defense and affect. The lateral septum (LS) has been implicated in the generation of the hippocampal theta rhythm, but its precise role in this process is not well understood. Here, we investigated the effects of direct pharmacological inhibition or disinhibition of the dorsal LS (dLS) on the frequency of hippocampal theta activity elicited by stimulation of the reticular formation in urethane-anesthetized rats. We found that bilateral infusions of the GABA A receptor agonist muscimol into the dLS significantly increased theta frequency. Strikingly, intra-dLS infusions of the GABA A receptor antagonist GABAzine largely abolished reticularly elicited theta activity. We also locally injected these same compounds into the medial septum (MS) to test for neuroanatomical specificity. In contrast to the effects seen in the dLS, intra-MS infusions of muscimol had no effect on theta frequency, whereas intra-MS infusions of GABAzine increased theta frequency. Given the hypothesized role of hippocampal theta in behavioral defense, we also examined the effects of intra-dLS application of muscimol in two models of anxiety, the elevated plus maze and the novelty-induced suppression of feeding paradigm; both tests revealed clear, anxiolytic-like effects following muscimol infusions. The fact that dLS-muscimol increased theta frequency while also reducing anxiety-like behaviors challenges the influential theta suppression model of anxiolysis, which predicts a slowing of theta with anxiolytic compounds. More importantly, the experiments reveal a novel role of the LS, especially its dorsal aspects, as an important gating mechanism for the expression of theta oscillations in the rodent hippocampus.

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Section: Discussionsupporting

confidence: 91%

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confidence: 99%

The lateral septum as a regulator of hippocampal theta oscillations and defensive behavior in rats

Chee

Menard

Dringenberg

2015

Journal of Neurophysiology

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“…Notably, very high densities of RLN3/RXFP3 were observed within the hippocampus and regions that regulate its function, including the medial septum/nucleus of the diagonal band, posterior hypothalamus, and supramammillary, interpeduncular, and median raphé nuclei, which together constitute the septohippocampal pathway (see e.g., Vertes, 1981;Vertes and Kocsis, 1997;Kirk, 1998;Pedemonte et al, 1998;Woodnorth et al, 2003;Woodnorth and McNaughton, 2005;Jackson et al, 2008). High levels of RLN3/RXFP3 were also observed in arousal-related brain areas, such as the raphé nuclei, lateral hypothalamus, and periaqueductal gray, while lower levels were present in other arousal structures, such as the ventral tegmental area and the pedunculopontine tegmental nucleus (see e.g., Mieda and Yanagisawa, 2002;Saper et al, 2005;Lu et al, 2006;Monti and Jantos, 2008).…”

Section: Discussionmentioning

confidence: 99%

Distribution of relaxin‐3 and RXFP3 within arousal, stress, affective, and cognitive circuits of mouse brain

Smith

Shen

Banerjee

et al. 2010

J of Comparative Neurology

137

264

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Relaxin-3 (RLN3) and its native receptor, relaxin family peptide 3 receptor (RXFP3), constitute a newly identified neuropeptide system enriched in mammalian brain. The distribution of RLN3/RXFP3 networks in rat brain and recent experimental studies suggest a role for this system in modulation of arousal, stress, metabolism, and cognition. In order to facilitate exploration of the biology of RLN3/RXFP3 in complementary murine models, this study mapped the neuroanatomical distribution of the RLN3/RXFP3 system in mouse brain. Adult, male wildtype and RLN3 knock-out (KO)/LacZ knock-in (KI) mice were used to map the central distribution of RLN3 gene expression and RLN3-like immunoreactivity (-LI). The distribution of RXFP3 mRNA and protein was determined using [(35)S]-oligonucleotide probes and a radiolabeled RXFP3-selective agonist ([(125)I]-R3/I5), respectively. High densities of neurons expressing RLN3 mRNA, RLN3-associated beta-galactosidase activity and RLN3-LI were detected in the nucleus incertus (or nucleus O), while smaller populations of positive neurons were observed in the pontine raphé, the periaqueductal gray and a region adjacent to the lateral substantia nigra. RLN3-LI was observed in nerve fibers/terminals in nucleus incertus and broadly throughout the pons, midbrain, hypothalamus, thalamus, septum, hippocampus, and neocortex, but was absent in RLN3 KO/LacZ KI mice. This RLN3 neural network overlapped the regional distribution of RXFP3 mRNA and [(125)I]-R3/I5 binding sites in wildtype and RLN3 KO/LacZ KI mice. These findings provide further evidence for the conserved nature of RLN3/RXFP3 systems in mammalian brain and the ability of RLN3/RXFP3 signaling to modulate "behavioral state" and an array of circuits involved in arousal, stress responses, affective state, and cognition.

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“…Numerous studies have confirmed that electrical stimulation of the MSA Garcia-Sanchez et al, 1978) or afferent inputs to the MSA including the reticular formation (Gaztelu and Buño, 1982), medial forebrain bundle (Brazhnik and Vinogradova, 1988), the lateral septum (Brazhnik et al, 1985;Pedemonte et al, 1998), and the fornix GarciaSanchez et al, 1978) all reset HPC theta. However, most of these studies primarily involved examining theta reset under anesthetized conditions.…”

Section: Introductionmentioning

confidence: 95%

Stimulation‐induced reset of hippocampal theta in the freely performing rat

Williams

Givens

2002

Hippocampus

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Previous research has suggested that visual and auditory stimuli in a working memory task have the ability to reset hippocampal theta, perhaps allowing an organism to encode the incoming information optimally. The present study examined two possible neural pathways involved in theta resetting. Rats were trained on a visual discrimination task in an operant chamber. At the beginning of a trial, a light appeared over a centrally located lever that the rat was required to press to receive a water reward. There was a 30-s intertrial interval before the next light stimulus appeared. After learning the task, all rats received surgical implantation of stimulating electrodes in both the fornix and the perforant path and recording electrodes, bilaterally in the hippocampus. After surgery, theta was recorded before and after the light stimulus to determine whether resetting to the visual stimulus occurred. During the intertrial interval, rats received single-pulse electrical stimulation of either the fornix or perforant path. Theta was recorded both before and after the electrical stimulation to determine whether resetting occurred. In this experiment, hippocampal theta was reset after all three stimulus conditions (light, perforant path, and fornix stimulation), with the greatest degree of reset occurring after the fornix stimulation. The results suggest that activation of the perforant path and fornix may underlie theta reset and provide a mechanism by which the hippocampus may enhance cognitive processing.

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Membrane and circuit properties of lateral septum neurons: relationships with hippocampal rhythms

Cited by 36 publications

References 36 publications

The lateral septum as a regulator of hippocampal theta oscillations and defensive behavior in rats

The lateral septum as a regulator of hippocampal theta oscillations and defensive behavior in rats

Distribution of relaxin‐3 and RXFP3 within arousal, stress, affective, and cognitive circuits of mouse brain

Stimulation‐induced reset of hippocampal theta in the freely performing rat

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