The fasciculus retroflexus controls the integrity of REM sleep by supporting the generation of hippocampal theta rhythm and rapid eye movements in rats

Valjakka, Antti; Vartiainen, Jukka; Tuomisto, Leena; Tuomisto, Jouni T.; Olkkonen, H.; Airaksinen, Mauno M.

doi:10.1016/s0361-9230(98)00006-9

Cited by 74 publications

(48 citation statements)

References 77 publications

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“…Hence, auditory gating is closely associated with sleep͞wake states, and it is thus reasonable to infer a functional link to brain areas that could influence these changes. Because many studies have shown that the MHb is such a sleep͞wake modulatory brain area (31,35,36), we propose that the MHb may play an important part in the auditory gating of the HVC and NIf by means of the Uva.…”

Section: Discussionmentioning

confidence: 98%

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Akutagawa

Konishi

2005

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

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The vocal control system of zebra finches shows auditory gating in which neuronal responses to the individual bird's own song vary with behavioral states such as sleep and wakefulness. However, we know neither the source of gating signals nor the anatomical connections that could link the modulatory centers of the brain with the song system. Two of the song-control nuclei in the forebrain, the HVC (used as the proper name) and the interfacial nucleus of the nidopallium, both show auditory gating, and they receive input from the uvaeform nucleus (Uva) in the thalamus. We used a combination of anterograde and retrograde tracing methods to show that the dorsal part of the reticular formation and the medial habenula (MHb) project to the Uva. We also show by choline acetyl transferase immunohistochemistry that the MHb is cholinergic and sends cholinergic fibers to the Uva. Our findings suggest that the Uva might serve as a hub to coordinate neuromodulatory input into the song system. auditory gating ͉ cholinergic ͉ song system ͉ thalamus T he song system is a discrete, interconnected series of brain nuclei in songbirds that controls singing, which is a learned vocal behavior ( Fig. 1) (1). In addition to displaying song motor activity, neurons of most song nuclei selectively respond to playback of the individual bird's own song (BOS) (2). Responses to the BOS are not created de novo in each song nucleus (3) but are relayed from the HVC to a vocal motor pathway that includes the robust nucleus of the arcopallium (RA) and the tracheosyringeal part of the hypoglossal nucleus. Auditory information also is transmitted from the HVC to an anterior forebrain pathway that includes area X within the songbird medial striatum; the nucleus dorsolateralis anterior thalami, pars medialis; the lateral magnocellular nucleus of the anterior nidopallium; and the RA. The source of auditory input to the HVC is thought to be the interfacial nucleus of the nidopallium (NIf), in which selectivity for the BOS is not as exclusive as in the HVC (4). Both the degree and selectivity of BOS-evoked responses in the HVC vary with natural and induced behavioral states such as sleeping, wakefulness, and anesthesia. This phenomenon is called ''auditory gating'' (5) and provides evidence that links the modulation of auditory input with the vocal control system. The first site of gating in the chain of song nuclei is thought to be the NIf (6). However, little is known about the source of signals that control gating in the NIf. Although several candidate sources for neural modulation have been postulated (7,8), the connections between these areas and the song system remain tenuous. The present study provides anatomical evidence that the uvaeform nucleus (Uva), which projects to both the NIf and HVC, receives cholinergic fibers from neurons in the medial habenula (MHb) and also afferents from the nucleus reticularis superior, pars dorsalis (RSd). These thalamic areas are neuromodulatory centers in other vertebrates, suggesting that the Uva in songbirds ma...

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Section: Discussionmentioning

confidence: 98%

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Akutagawa

Konishi

2005

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

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“…Unlike most brain regions, glucose utilization in the IP is increased during REM sleep as well as under anesthesia (24)(25)(26). Moreover, bilateral lesions of the fasciculus retroflexus, the major afferent path from the IP, decrease the time spent in REM sleep (6,7). To date, however, no report has directly examined the role of the IP in sleep mechanisms, primarily because research has tended to focus on the dorsal region of the brainstem (2-4) and because surgical procedures targeting the IP inevitably damage bilateral dorsal brainstem nuclei as well as fibers connecting the hypothalamus with the brainstem nuclei.…”

Section: Discussionmentioning

confidence: 99%

“…It has been reported that lesions of the bilateral fasciculus retroflexus, a major input to the interpeduncular nucleus (IP), result in reduced REM sleep time (6,7). The IP is located on the midline in the ventral region of the midbrain-hindbrain transition and is evolutionarily conserved from fish to mammals.…”

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confidence: 99%

Loss of Goosecoid-like and DiGeorge syndrome critical region 14 in interpeduncular nucleus results in altered regulation of rapid eye movement sleep

Funato

Sato²,

Sinton³

et al. 2010

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

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Sleep and wakefulness are regulated primarily by inhibitory interactions between the hypothalamus and brainstem. The expression of the states of rapid eye movement (REM) sleep and non-REM (NREM) sleep also are correlated with the activity of groups of REM-off and REM-on neurons in the dorsal brainstem. However, the contribution of ventral brainstem nuclei to sleep regulation has been little characterized to date. Here we examined sleep and wakefulness in mice deficient in a homeobox transcription factor, Goosecoid-like (Gscl), which is one of the genes deleted in DiGeorge syndrome or 22q11 deletion syndrome. The expression of Gscl is restricted to the interpeduncular nucleus (IP) in the ventral region of the midbrain-hindbrain transition. The IP has reciprocal connections with several cell groups implicated in sleep/wakefulness regulation. Although Gscl −/− mice have apparently normal anatomy and connections of the IP, they exhibited a reduced total time spent in REM sleep and fewer REM sleep episodes. In addition, Gscl −/− mice showed reduced theta power during REM sleep and increased arousability during REM sleep. Gscl −/− mice also lacked the expression of DiGeorge syndrome critical region 14 (Dgcr14) in the IP. These results indicate that the absence of Gscl and Dgcr14 in the IP results in altered regulation of REM sleep.homeobox transcription factor | mouse behavior | ventral brainstem

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“…The main efferent projection target of neurons in the septofimbrial and triangular septal nuclei is the medial habenula, which projects to the interpeduncular nuclei (Herkenham and Nauta, 1977) that in turn projects to the nucleus incertus (Goto et al, 2001), thus 'closing the anatomical/functional loop'. This circuit also appears to participate in theta rhythm regulation and associated phenomena, as transection of the fasciculus retroflexus tract connecting the habenula to the interpeduncular nucleus results in reduction of hippocampal theta and REM sleep (high levels of theta characterize REM sleep) (Haum et al, 1992;Valjakka et al, 1998).…”

Section: Implications For Understanding Lateral Septum Functionmentioning

confidence: 99%

Distribution and targets of the relaxin‐3 innervation of the septal area in the rat

Olucha-Bordonau¹,

Otero-García²,

Sánchez-Pérez³

et al. 2012

J of Comparative Neurology

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Neural tracing studies have revealed that the rat medial and lateral septum are targeted by ascending projections from the nucleus incertus, a population of tegmental GABA neurons. These neurons express the relaxin‐family peptide, relaxin‐3, and pharmacological modulation of relaxin‐3 receptors in medial septum alters hippocampal theta rhythm and spatial memory. In an effort to better understand the basis of these interactions, we have characterized the distribution of relaxin‐3 fibers/terminals in relation to different septal neuron populations identified using established protein markers. Dense relaxin‐3 fiber plexuses were observed in regions of medial septum containing hippocampal‐projecting choline acetyltransferase (ChAT)‐, neuronal nitric oxide synthase (nNOS)‐, and parvalbumin (PV)‐positive neurons. In lateral septum (LS), relaxin‐3 fibers were concentrated in the ventrolateral nucleus of rostral LS and the ventral nucleus of caudal LS, with sparse labeling in the dorsolateral and medial nuclei of rostral LS, dorsal nucleus of caudal LS, and ventral portion nuclei. Relaxin‐3 fibers were also observed in the septofimbrial and triangular septal nuclei. In the medial septum, we observed relaxin‐3‐immunoreactive contacts with ChAT‐, PV‐, and glutamate decarboxylase‐67‐positive neurons that projected to hippocampus, and contacts between relaxin‐3 terminals and calbindin‐ and calretinin‐positive neurons. Relaxin‐3 colocalized with synaptophysin in nerve terminals in all septal areas, and ultrastructural analysis revealed these terminals were symmetrical and contacted spines, somata, dendritic shafts, and occasionally other axonal terminals. These data predict that this GABA/peptidergic projection modulates septohippocampal activity and hippocampal theta rhythm related to exploratory navigation, defensive and ingestive behaviors, and responses to neurogenic stressors. J. Comp. Neurol. 520:1903–1939, 2012. © 2011 Wiley Periodicals, Inc.

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The fasciculus retroflexus controls the integrity of REM sleep by supporting the generation of hippocampal theta rhythm and rapid eye movements in rats

Cited by 74 publications

References 77 publications

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Connections of thalamic modulatory centers to the vocal control system of the zebra finch

Loss of Goosecoid-like and DiGeorge syndrome critical region 14 in interpeduncular nucleus results in altered regulation of rapid eye movement sleep

Distribution and targets of the relaxin‐3 innervation of the septal area in the rat

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