The functional relationship between septal and hippocampal unit activity and hippocampal theta rhythm

Macadar, O.; Roig, J.A.; Monti, J.M.; Budelli, Rubén

doi:10.1016/0031-9384(70)90134-4

Cited by 111 publications

(34 citation statements)

References 11 publications

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“…Significance levels are labeled only when the value of the pair from 2 pro-arousal slow-firing neurons is significantly larger than that of any other types of pairs. ⌬P Ͻ 0.05; ϩP Ͻ 0.01; #P Ͻ 0.001. ical properties in isolated domains, e.g., firing rate modulations in all major arousal states (Morales et al 1971;Sweeney et al 1992), responses to behavioral events (Mercer and Remley 1979;Zin et al 1977), and intrinsic firing properties in relation to theta oscillations (King et al 1998;Macadar et al 1970;Petsche et al 1962). The lack of comprehensive characterization across those feature domains has made it difficult to compare and integrate results collected in different studies.…”

Section: A Distinctive Putatively Cholinergic Subpopulation Of Neuromentioning

confidence: 99%

A distinctive subpopulation of medial septal slow-firing neurons promote hippocampal activation and theta oscillations

Zhang

Lin

Nicolelis

2011

Journal of Neurophysiology

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Although many previous studies have focused on understanding how MSVDB neurons fire rhythmic bursts to pace hippocampal theta oscillations, a significant portion of MSVDB neurons are slow-firing and thus do not pace theta oscillations. The function of these MSVDB neurons, especially their role in modulating hippocampal activity, remains unknown. We recorded MSVDB neuronal ensembles in behaving rats, and identified a distinct physiologically homogeneous subpopulation of slow-firing neurons (overall firing Ͻ4 Hz) that shared three features: 1) much higher firing rate during rapid eye movement sleep than during slow-wave (SW) sleep; 2) temporary activation associated with transient arousals during SW sleep; 3) brief responses (latency 15ϳ30 ms) to auditory stimuli. Analysis of the fine temporal relationship of their spiking and theta oscillations showed that unlike the theta-pacing neurons, the firing of these "pro-arousal" neurons follows theta oscillations. However, their activity precedes short-term increases in hippocampal oscillation power in the theta and gamma range lasting for a few seconds. Together, these results suggest that these pro-arousal slow-firing MSvDB neurons may function collectively to promote hippocampal activation. medial septum; small-amplitude irregular activity, auditory response; theta oscillations; cholinergic THE MEDIAL SEPTUM-VERTICAL LIMB of the diagonal band of Broca (MSvDB) heavily innervates the hippocampus through cholinergic, GABAergic, and glutamatergic projections (Gritti et al. 2006;Kiss et al. 1990;Kohler et al. 1984;Lewis et al. 1967). These projections are essential for normal hippocampal functions. Lesion or inactivation of MSvDB recapitulates the memory deficit resulting from hippocampal lesions and eliminates hippocampal theta oscillations (Gray and McNaughton 1983;Green and Arduini 1954;Mahut 1972;Mizumori et al. 1990;Winson 1978).To achieve a mechanistic understanding of the critical role of MSvDB in hippocampal functioning, it is essential to elucidate how the neuronal activity in MSvDB modulates hippocampal activity, in particular its dynamic interactions on fine temporal scales. Indeed, this issue has been studied extensively at the electrophysiological level over the last few decades. Those studies have largely focused on the fast-firing, rhythmic-bursting MSvDB neurons and have demonstrated that these cells are the pacemaker of hippocampal theta oscillations (Ford et al. 1989;Hangya et al. 2009;Morales et al. 1971;Petsche et al. 1962).However, in parallel with their heterogeneity in terms of neurotransmitters, the physiological properties of MSvDB neurons are similarly diverse. In addition to the extensively studied fast-firing, rhythmic-bursting neurons, many MSvDB neurons are nonetheless slow-firing and do not fire theta-range rhythmic bursts (Ford et al. 1989;Gaztelu and Buno 1982;Stewart and Fox 1989). As such, these latter cells are unlikely candidates to participate in pacing theta oscillations. The function of these slow-firing neurons remains unknown, in ...

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Section: A Distinctive Putatively Cholinergic Subpopulation Of Neuromentioning

confidence: 99%

A distinctive subpopulation of medial septal slow-firing neurons promote hippocampal activation and theta oscillations

Zhang

Lin

Nicolelis

2011

Journal of Neurophysiology

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“…These pathways generate rhythmic activity of various frequencies (14)(15)(16)(17)(18), some aspects of which can be reproduced in hippocampal slices by infusing cholinergic agonists (19)(20)(21)(22)(23). The in vitro rhythms are mediated by mAChRs (19,20,22,23) and originate in the CA3 region from whence they move along intrahippocampal pathways to other subfields (22,23).…”

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confidence: 99%

Cholinergic plasticity in the hippocampus

Colgin¹,

Kubota

Lynch

2003

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

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Tests were made for use-dependent plasticity in the cholinergic projections to hippocampus. Transient infusion of the cholinergic agonist carbachol into hippocampal slices induced rhythmic activity that persisted for hours after washout. Comparable effects were obtained with physostigmine, a drug that blocks acetylcholine breakdown and thereby enhances cholinergic transmission. It thus seems that activation of cholinergic synapses induces lasting changes in hippocampal physiology. Two lines of evidence indicated that cholinergic synapses are also the sites at which the plasticity is expressed. First, the induction and expression of the rhythms were not blocked by the N-methyl-D-aspartate receptor antagonist D-2-amino-5-phosphonovaleric acid, indicating that a long-term potentiation effect between pyramidal cells was not involved. Second, a muscarinic antagonist (atropine) completely abolished stable rhythmic activity after agonist washout. This result indicates that endogenous cholinergic activity is responsible for the persistence of rhythmic oscillations. These experiments suggest that short periods of intense cholinergic activity induce lasting changes in cholinergic synapses and thus extend such forms of plasticity to beyond the glutamatergic system.

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“…The results of the present studies seem to support this suggestion. An alternative to the fear-attenuation explanation that would account for the present results may be based on the findings that various septal nuclei have both efferent and afferent connections to other subcortical regions, particularly to hippocampus (Carey, 1968;Lewis & Shute, 1967;Macadar, Roig, Monti, & Budelli, 1970;Petsche, Stumpf, Gogolack, 1962;Petsche, Gogolack, & Van Zwieten, 1965;Powell, 1966;Raisman, 1966;Raisman, Cowan, & Powell, 1966). Accordingly, each of these structures may function as a sort of relay station for the other (cf.…”

Section: Discussionmentioning

confidence: 86%

Septal lesion effects on a two-way avoidance task with one-way avoidance task characteristics: A test of a fear-attenuation hypothesis

1980

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Two experiments were conducted to assess the hypothesis that septal lesions result in a decrement in conditioned fear and to investigate whether the different effects of septal lesions in one-way and two-way avoidance tasks are due to some procedural differences between these two tasks_ Experiment 1 compared the septal and normal control rats in a two-way avoidance task that incorporated a safe platform under the subject after a response but did not involve handling the subject (one-way analogue task). Experiment 2 investigated the effects of septal lesions in conventional two-way and one-way analogue tasks with two levels of shock intensity. The results indicated that, in the absence of a moving partition or electrified grids on top of the hurdle, the one-way analogue task enhanced the performance of both the normals and septa Is with both levels of shock intensity. Shock intensity had no effect in the one-way analogue task, but the more intense shock degraded the performance of both septals and normals in the two-way task. These results are not predicted by the fear-attenuation hypothesis. An alternative hypothesis in terms of the septals' deficiency in the utilization of spatial cues was tested and shown able to account for all of the present results.

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The functional relationship between septal and hippocampal unit activity and hippocampal theta rhythm

Cited by 111 publications

References 11 publications

A distinctive subpopulation of medial septal slow-firing neurons promote hippocampal activation and theta oscillations

A distinctive subpopulation of medial septal slow-firing neurons promote hippocampal activation and theta oscillations

Cholinergic plasticity in the hippocampus

Septal lesion effects on a two-way avoidance task with one-way avoidance task characteristics: A test of a fear-attenuation hypothesis

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