Responses of the suprachiasmatic nucleus to retinohypothalamic tract volleys in a slice preparation of the mouse hypothalamus

doi:10.1016/0006-8993(89)91336-X

Brain Research

Volume 479, Issue 1, 6 February 1989, Pages 65-75

https://doi.org/10.1016/0006-8993(89)91336-X Get rights and content

Abstract

The electrophysiological responses of the mouse suprachiasmatic nucleus (SCN) to stimulated synaptic input from the retinohypothalamic tract (RHT) were investigated using a hypothalamic slice preparation that includes the entire SCN, optic chiasm and optic nerves. Extracellular recording of single-unit activity reveal a population of neurons in the ventrolateral SCN that are activated at a median latency of 10 ms after stimulation of the contralateral optic nerve. These neurons apparently receive direct excitatory input from RHT synapses. Other SCN neurons are activated at longer latencies, possibly through input from interneurons. The population field potentials evoked in the SCN by optic nerve volleys consist of a calcium-insensitive transient generated by optic tract axons in the chiasm, followed by calcium-sensitive waves generated by postsynaptic activity. The postsynaptic waves have the form of a field EPSP, negative in the dorsolateral SCN and positive in the ventrolateral SCN, upon which is superimposed a population spike of opposite polarity. The population spike occurs at the same latency as the monosynaptic single unit responses, which were all found near or ventral to the point of reversal of field potential. These findings suggest that neurons in the ventrolateral SCN are excited by synapses on dorsally extended dendrites. The conduction velocity of the RHT in the optic nerve was found to be 0.59 ± 0.03 mm/ms, while that of the optic tract volley was 2.4 ± 0.75 mm/ms. The low conduction velocity of the RHT indicates that, within the optic nerve, these axons are thin and/or unmyelinated in the optic nerve.

References (20)

D.C. Klein et al.
Pineal N-acetyltransferase and hydroxyindole-o-methyltransferase: control by the retinohypothalamic tract and the suprachiasmatic nucleus
Brain Research
(1979)
H. Nishino et al.
The role of the suprachiasmatic nucleus of the hypothalamus in the production of circadian rhythm
Brain Research
(1976)
G.E. Pickard
Bifurcating axons of retinal ganglion cells terminate in the hypothalamic suprachiasmatic nucleus and the intergeniculate leaflet of the thalamus
Neurosci. Lett.
(1985)
S. Shibata et al.
Responses of suprachiasmatic nucleus neurons to optic nerve stimulation in rat hypothalamic slice preparation
Brain Research
(1984)
S. Shibata et al.
Field potentials in the suprachiasmatic nucleus of the rat hypothalamic slice produced by optic nerve stimulation
Brain Res. Bull.
(1984)
T.G. Youngstrom et al.
Comparative anatomy of the retinohypothalamic tract in photoperiodic and non-photoperiodic rodents
Brain Res. Bull.
(1986)
P. Anderson et al.
Unit analysis of hippocampal population spikes
Exp. Brain Res.
(1971)
R.E. Foster et al.
Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development
Dev. Brain Res.
(1982)
G.A. Groos et al.
Electrical and pharmacological properties of the suprachiasmatic nuclei
F.H. Guldner
Synapses of optic nerve afferents in the rat suprachiasmatic nucleus. I. Identification, qualitative description, development and distribution
Cell Tiss. Res.
(1978)

There are more references available in the full text version of this article.

Cited by (34)

Imaging the Role of Myelin in Concussion
2018, Neuroimaging Clinics of North America
Citation Excerpt :
Although myelin decompaction may not be as severe an injury as myelin degeneration, there is still reason to view these changes as a serious mTBI disorder, because they lead to reductions in action potential conduction.59 Myelinated axons in mice and rats have been found to conduct at a rate of 2.4 m/s, which is significantly greater than the unmyelinated rate of 0.4 m/s.60,61 Axons of mice with decompacted myelin conduct at a rate of about 1.05 m/s.59 This difference represents a reduction of more than half the conduction rate, and could in turn be responsible for some of the known cognitive deficits following mTBI,62 such as affected memory, attention, processing speed, and executive functioning. As discussed earlier, myelin decompaction in mTBI is likely to be caused by secondary mechanisms, such as oxidative stress.25
Enrichment of glutamate-like immunoreactivity in the retinotectal terminals of the viper Vipera aspis: An electron microscope quantitative immunogold study
1997, Journal of Chemical Neuroanatomy
A post-embedding immunogold study was carried out to estimate the immunoreactivity to glutamate in retinal terminals, P axon terminals and dendrites containing synaptic vesicles in the superficial layers of the optic tectum of Vipera. Retinal terminals, identified following either intraocular injection of tritiated proline, horseradish peroxidase (HRP) or short-term survivals after retinal ablation, were observed to be highly glutamate-immunoreactive. A detailed quantitative analysis showed that about 50% of glutamate immunoreactivity was localized over the synaptic vesicles, 35.8% over mitochondria and 14.2% over the axoplasmic matrix. The close association of immunoreactivity with the synaptic vesicles could indicate that Vipera retino-tectal terminals may use glutamate as their neurotransmitter. P axon terminals and dendrites containing synaptic vesicles, strongly γ-aminobutyric (GABA)-immunoreactive, were shown to be also moderately glutamate-immunoreactive, but two to three times less than retinal terminals. Moreover, in P axon terminals, the glutamate immunoreactivity was denser over mitochondria than over synaptic vesicles, possibly reflecting the `metabolic' pool of glutamate, which serves as a precursor in the formation of GABA.
In vitro stimulation of c-Fos protein expression in the suprachiasmatic nucleus of hypothalamic slices
1996, Molecular Brain Research
Light regulates the c-fos protooncogene in the suprachiasmatic nucleus (SCN), with increased expression after animals are exposed to light during the dark phase of a light-dark cycle or during the subjective night in constant darkness. To determine whether this phase-dependent activation of c-Fos persists in an acute in vitro preparation, we prepared horizontal slices of hamster ventral hypothalamus, electrically stimulated the still-attached optic nerves, recorded the resulting evoked pontentials in the SCN, and examined c-Fos protein levels in the nucleus by immunohistochemistry. The number of SCN cells labeled for immunoreactive c-Fos was significantly increased in slices stimulated during projected night, but not during projected day, compared to matched, sham-stimulated control slices. These results imply that the phase-dependent mechanism that gates c-Fos photoinduction in vivo is intrinsic to SCN tissue, and they suggest that an in vitro slice preparation will provide a useful model for dissecting the responsible signal transduction elements.
Decompaction of CNS myelin leads to a reduction of the conduction velocity of action potentials in optic nerve
1995, Neuroscience Letters
The conduction velocity of action potentials in nerve fibres is proportional to the degree of myelination. Here we studied the influence of myelin ultrastructure on the compound action potential conduction velocity in optic nerves of the proteolipid protein (PLP)-deficient mouse model, which displays loose myelination in central fibres. We show that a myelin decompaction leads to a suboptimal conduction velocity. The significance of myelin ultrastructure for conduction of action potential in the optic nerve is discussed.
Neurochemical organization of circadian rhythm in the suprachiasmatic nucleus
1994, Neuroscience Research
The circadian rhythm in mammals is under control of the pacemaker located in the suprachiasmatic nucleus (SCN) of the hypothalamus. This tiny nucleus contains a number of neurochemicals, including peptides, amines and amino acids. Heterogeneous distribution of these neurochemicals defines the substructures of the SCN. In the present review, functional significance of such neurochemical heterogeneity in the SCN is discussed in the light of circadian patterns of the concentrations of these neurochemicals in the SCN and their effects on SCN neurons in in vitro slice preparation. In particular, the hypothesis that the dorsomedial SCN is involved in maintaining the circadian rhythm, while the ventrolateral SCN is involved in adjusting the phase of the rhythm, is critically discussed. These considerations suggest that distinct sub-components of the SCN as marked by neurochemicals, interact with each other and this organizational architecture could be the basis of the proper operation of the circadian time keeping system in this nucleus.
Fast multisite optical recording of mono- and polysynaptic activity in the hamster suprachiasmatic nucleus evoked by retinohypothalamic tract stimulation
1994, NeuroImage
Responses of the hamster suprachiasmatic nucleus (SCN) to retinohypothalamic tract (RHT) stimulation were studied in horizontal hypothalamic slices using fast multisite optical recording techniques. A 124-element photodiode detector array provided high-speed monitoring (0.5 ms/frame) of evoked neural activity in the SCN, while a larger 464-element photodiode array yielded improved spatial imaging with some loss in temporal resolution (1.6 ms/frame). Brief electrical stimulation of the optic nerves evoked a propagated compound action potential that was recorded optically as a single transient depolarization in many slice regions, including the SCN. Only within the SCN, however, was this optic tract signal followed by additional voltage-dependent optical responses which exhibited a fast and a slow depolarizing component. The initial upstroke of the fast component was Ca²⁺-insensitive and is presumed to reflect activity in presynaptic RHT afferents. The remainder of the fast depolarization and the slow depolarization were Ca²⁺-sensitive.These responses were labeled the early population excitatory postsynaptic potential (Early P.E.P.S.P.) and the Late P.E.P.S.P. respectively. The Late P.E.P.S.P. was not enhanced by K⁺ channel blockade, suggesting that glial depolarization is not the primary source of this component. Drugs known to suppress RHT-evoked SCN field potentials also suppressed the Early and Late P.E.P.S.P.'s recorded optically in the SCN. Unexpectedly, the Early P.E.P.S.P. was also reduced by the GABA_A antagonist, bicuculline. Surface plots of normalized peak amplitudes showed that both SCN components had similar spatial distributions within the SCN, although the Early P.E.P.S.P. tended to be slightly more prominent within the medial SCN in some preparations. It is suggested that the Early P.E.P.S.P. represents firing of monosynaptically activated SCN neuron`s, while the Late P.E.P.S.P. reflects polysynaptic activity within the intrinsic SCN neuronal network that may be involved in the light entrainment of the circadian oscillator.

View all citing articles on Scopus

^∗: Present address: M. Menaker, Department of Biology, University of Virginia, Charlottesville, VA 22901, U.S.A.

View full text

Research reportResponses of the suprachiasmatic nucleus to retinohypothalamic tract volleys in a slice preparation of the mouse hypothalamus

Abstract

Brain Research

Brain Research

Neurosci. Lett.

Brain Research

Brain Res. Bull.

Brain Res. Bull.

Unit analysis of hippocampal population spikes

Exp. Brain Res.

Rat optic nerve: electrophysiological, pharmacological and anatomical studies during development

Dev. Brain Res.

Electrical and pharmacological properties of the suprachiasmatic nuclei

Synapses of optic nerve afferents in the rat suprachiasmatic nucleus. I. Identification, qualitative description, development and distribution

Cell Tiss. Res.

Research report
Responses of the suprachiasmatic nucleus to retinohypothalamic tract volleys in a slice preparation of the mouse hypothalamus