A comparison of supramammillary and medial septal influences on hippocampal field potentials and single-unit activity

S. J Y Mizumori, B. L. McNaughton, Carol A Barnes

Research output: Contribution to journalArticle

117 Citations (Scopus)

Abstract

A comparison was made between the influences of supramammillary (SUM) and medial septal (MS) nuclei on hippocampal physiology in Nembutal-anesthetized rats. Specifically, the effects of prestimulation of the SUM or MS on the perforant path-dentate field potential, on spontaneous activity of single units, and on perforant path-induced unit activation were assessed. Another series of experiments addressed the issue of whether the SUM and MS effects on the perforant path-dentate field response are independent. Prestimulation of the SUM or MS significantly facilitated the perforant path-dentate population spike with no clear effect on the field excitatory postsynaptic potential (EPSP) recorded in the subgranular zone of the dentate hilus. Prestimulation of either nucleus also reduced the threshold for spike onset. The major differences between the two spike facilitation effects were the magnitude of the change and possibly the optimal interstimulus intervals required to obtain the effects. Acute transection of the ipsilateral column of fornix or dorsal fornix eliminated the SUM population spike facilitation effect. MS lesion or dorsal fornix/fimbria transection eliminated the MS spike facilitation effect. The MS lesion did not alter the effects of SUM prestimulation. Cingulum or medial forebrain bundle transection affected neither SUM- nor MS-mediated spike facilitation. Thus the SUM and MS influences on the dentate field response appear to be independent of one another. The relevant SUM afferents travel through the ipsilatral column of fornix and dorsal fornix, whereas MS afferents project through the dorsal fornix/fimbria. Single units recorded in stratum granulosum (SG) were assessed with respect to several parameters. These included the mean firing rate, whether or not excitation occurred prior to the field population spike and at lower threshold, and whether or not a driven unit respond to a second perforant path stimulus delivered at short latency following the first (during the period of population spike depression). The latter parameter in particular appeared to separate SG cells into two classes. The cells that were not activated during the second field potential were classified as granule cells, whereas those that were activated were classified as basket cells. Based on this distinction, significant differences were also found between the two cell classes on the other parameters. In particular, cells classified as granule cells often had very low firing rates. We conclude that many previous studies have mistakenly identified as granule cells inhibitory interneurons, which are much more commonly encountered (at least partly due to their higher discharge rates). This misidentification has led to several hypotheses concerning the mechanism of heterosynaptically induce population spike facilitation that we now conclude are untenable. Stimulation of the SUM or MS alone resulted in a reduction in the spontaneous firing rate of more than one-half of the cells recorded in the SG. Based on one or more of the above criteria, these cells were classified as basket cells. Also, stimulation of the SUM or MS prior to perforant path stimulation significantly reduced the probability of basket cell activation by the perforant path stimulus. Roughly 15% of SG cells recorded showed increased firing in response to SUM or MS stimulation. These cells had very low spontaneous rats and were therefore classified as granule cells. Relatively little change was observed in the firing rates of CA1, CA3, or hilar complex-spike cells. Roughly equal proportions of CA1 theta cells responsed with reduced or elevated firing. Thus, although additional mechanisms may also contribute, the heterosynaptic facilitation of the granule cell population spike is probably largely due to the suppression of inhibitory interneurons, as orginally suggested by Bilkey and Goddard for the MS-induced effect, on the basis of field potential studies.

Original languageEnglish (US)
Pages (from-to)15-31
Number of pages17
JournalJournal of Neurophysiology
Volume61
Issue number1
StatePublished - 1989
Externally publishedYes

Fingerprint

Perforant Pathway
Brain Fornix
Population
Granulosa Cells
Interneurons
Medial Forebrain Bundle
Septal Nuclei
Excitatory Postsynaptic Potentials
Pentobarbital

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

A comparison of supramammillary and medial septal influences on hippocampal field potentials and single-unit activity. / Mizumori, S. J Y; McNaughton, B. L.; Barnes, Carol A.

In: Journal of Neurophysiology, Vol. 61, No. 1, 1989, p. 15-31.

Research output: Contribution to journalArticle

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abstract = "A comparison was made between the influences of supramammillary (SUM) and medial septal (MS) nuclei on hippocampal physiology in Nembutal-anesthetized rats. Specifically, the effects of prestimulation of the SUM or MS on the perforant path-dentate field potential, on spontaneous activity of single units, and on perforant path-induced unit activation were assessed. Another series of experiments addressed the issue of whether the SUM and MS effects on the perforant path-dentate field response are independent. Prestimulation of the SUM or MS significantly facilitated the perforant path-dentate population spike with no clear effect on the field excitatory postsynaptic potential (EPSP) recorded in the subgranular zone of the dentate hilus. Prestimulation of either nucleus also reduced the threshold for spike onset. The major differences between the two spike facilitation effects were the magnitude of the change and possibly the optimal interstimulus intervals required to obtain the effects. Acute transection of the ipsilateral column of fornix or dorsal fornix eliminated the SUM population spike facilitation effect. MS lesion or dorsal fornix/fimbria transection eliminated the MS spike facilitation effect. The MS lesion did not alter the effects of SUM prestimulation. Cingulum or medial forebrain bundle transection affected neither SUM- nor MS-mediated spike facilitation. Thus the SUM and MS influences on the dentate field response appear to be independent of one another. The relevant SUM afferents travel through the ipsilatral column of fornix and dorsal fornix, whereas MS afferents project through the dorsal fornix/fimbria. Single units recorded in stratum granulosum (SG) were assessed with respect to several parameters. These included the mean firing rate, whether or not excitation occurred prior to the field population spike and at lower threshold, and whether or not a driven unit respond to a second perforant path stimulus delivered at short latency following the first (during the period of population spike depression). The latter parameter in particular appeared to separate SG cells into two classes. The cells that were not activated during the second field potential were classified as granule cells, whereas those that were activated were classified as basket cells. Based on this distinction, significant differences were also found between the two cell classes on the other parameters. In particular, cells classified as granule cells often had very low firing rates. We conclude that many previous studies have mistakenly identified as granule cells inhibitory interneurons, which are much more commonly encountered (at least partly due to their higher discharge rates). This misidentification has led to several hypotheses concerning the mechanism of heterosynaptically induce population spike facilitation that we now conclude are untenable. Stimulation of the SUM or MS alone resulted in a reduction in the spontaneous firing rate of more than one-half of the cells recorded in the SG. Based on one or more of the above criteria, these cells were classified as basket cells. Also, stimulation of the SUM or MS prior to perforant path stimulation significantly reduced the probability of basket cell activation by the perforant path stimulus. Roughly 15{\%} of SG cells recorded showed increased firing in response to SUM or MS stimulation. These cells had very low spontaneous rats and were therefore classified as granule cells. Relatively little change was observed in the firing rates of CA1, CA3, or hilar complex-spike cells. Roughly equal proportions of CA1 theta cells responsed with reduced or elevated firing. Thus, although additional mechanisms may also contribute, the heterosynaptic facilitation of the granule cell population spike is probably largely due to the suppression of inhibitory interneurons, as orginally suggested by Bilkey and Goddard for the MS-induced effect, on the basis of field potential studies.",
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N2 - A comparison was made between the influences of supramammillary (SUM) and medial septal (MS) nuclei on hippocampal physiology in Nembutal-anesthetized rats. Specifically, the effects of prestimulation of the SUM or MS on the perforant path-dentate field potential, on spontaneous activity of single units, and on perforant path-induced unit activation were assessed. Another series of experiments addressed the issue of whether the SUM and MS effects on the perforant path-dentate field response are independent. Prestimulation of the SUM or MS significantly facilitated the perforant path-dentate population spike with no clear effect on the field excitatory postsynaptic potential (EPSP) recorded in the subgranular zone of the dentate hilus. Prestimulation of either nucleus also reduced the threshold for spike onset. The major differences between the two spike facilitation effects were the magnitude of the change and possibly the optimal interstimulus intervals required to obtain the effects. Acute transection of the ipsilateral column of fornix or dorsal fornix eliminated the SUM population spike facilitation effect. MS lesion or dorsal fornix/fimbria transection eliminated the MS spike facilitation effect. The MS lesion did not alter the effects of SUM prestimulation. Cingulum or medial forebrain bundle transection affected neither SUM- nor MS-mediated spike facilitation. Thus the SUM and MS influences on the dentate field response appear to be independent of one another. The relevant SUM afferents travel through the ipsilatral column of fornix and dorsal fornix, whereas MS afferents project through the dorsal fornix/fimbria. Single units recorded in stratum granulosum (SG) were assessed with respect to several parameters. These included the mean firing rate, whether or not excitation occurred prior to the field population spike and at lower threshold, and whether or not a driven unit respond to a second perforant path stimulus delivered at short latency following the first (during the period of population spike depression). The latter parameter in particular appeared to separate SG cells into two classes. The cells that were not activated during the second field potential were classified as granule cells, whereas those that were activated were classified as basket cells. Based on this distinction, significant differences were also found between the two cell classes on the other parameters. In particular, cells classified as granule cells often had very low firing rates. We conclude that many previous studies have mistakenly identified as granule cells inhibitory interneurons, which are much more commonly encountered (at least partly due to their higher discharge rates). This misidentification has led to several hypotheses concerning the mechanism of heterosynaptically induce population spike facilitation that we now conclude are untenable. Stimulation of the SUM or MS alone resulted in a reduction in the spontaneous firing rate of more than one-half of the cells recorded in the SG. Based on one or more of the above criteria, these cells were classified as basket cells. Also, stimulation of the SUM or MS prior to perforant path stimulation significantly reduced the probability of basket cell activation by the perforant path stimulus. Roughly 15% of SG cells recorded showed increased firing in response to SUM or MS stimulation. These cells had very low spontaneous rats and were therefore classified as granule cells. Relatively little change was observed in the firing rates of CA1, CA3, or hilar complex-spike cells. Roughly equal proportions of CA1 theta cells responsed with reduced or elevated firing. Thus, although additional mechanisms may also contribute, the heterosynaptic facilitation of the granule cell population spike is probably largely due to the suppression of inhibitory interneurons, as orginally suggested by Bilkey and Goddard for the MS-induced effect, on the basis of field potential studies.

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