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Comparative Study
.2006 Oct 4;26(40):10292-8.
doi: 10.1523/JNEUROSCI.2341-06.2006.

Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse

Affiliations
Comparative Study

Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse

Kazumi Takahashi et al. J Neurosci..

Abstract

Using extracellular single-unit recordings alone and in combination with neurobiotin juxtacellular labeling and histamine immunohistochemistry, we have identified, for the first time in nonanesthetized, head-restrained mice, histamine neurons in the tuberomammillary nuclei of the posterior hypothalamus. They are all characterized by triphasic broad action potentials. They are active only during wakefulness, and their activity is related to a high level of vigilance. During waking states, they display a slow (<10 Hz) tonic, repetitive, irregular firing pattern. Their activity varies in the different waking states, being lowest during quiet waking, moderate during active waking, and highest during attentive waking. They cease firing during quiet waking before the onset of EEG synchronization, the EEG sign of sleep (drowsy state), and remain silent during slow-wave sleep and paradoxical (or rapid eye movement) sleep. They exhibit a pronounced delay in firing during transitions from sleep to wakefulness or remain quiescent during the same transitions if the animals are not fully alert. They either respond with a long delay, or do not respond, to an arousing stimulus if the stimulus does not elicit an overt alert state. These data support the view that the activity of histaminergic tuberomammillary neurons plays an important role, not in the induction of wakefulness per se, but in the maintenance of the high level of vigilance necessary for cognitive processes. Conversely, cessation of their activity may play an important role in both the initiation and maintenance of sleep.

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Figures

Figure 1.
Figure 1.
Camera lucida drawings of frontal sections (four different planes at 0.2 mm intervals rostral to caudal) showing the distribution of HA-immunoreactive neurons (dots on the left side) and that of waking-specific neurons (white and black triangles on the right side), waking-active neurons (white and black circles on the right side), and other Nb-labeled non-HA neurons (dots on the right side). The white triangles and circles indicate cells from which recordings were made but which were not tested for Nb labeling and subsequent identification of neurotransmitter content. The black triangles indicate waking-specific neurons labeled with both Nb and HA. The black circles indicate waking-active neurons labeled with Nb but immunonegative for HA. 3V, Third ventricle; Arc, arcuate nucleus; Br, bregma; cp, cerebral peduncle; DM, dorsomedial hypothalamic nucleus; DTM, diffuse tuberomammillary nucleus; MTM, medial tuberomammillary nucleus; VTM, ventral tuberomammillary nucleus; f, fornix; MM medial mammillary nucleus; LM, lateral mammillary nucleus; mt, mammillothalamic tract; MTu, medial tuberal nucleus; PH, posterior hypothalamic area; pm, principal mammillary tract; PMV, ventral premammillary nucleus; STh, subthalamic nucleus; SuMM, medial supramammillary nucleus.
Figure 2.
Figure 2.
HA and non-HA neurons marked with pontamine sky blue or labeled for HA in the TM.a, Photomicrographs showing the recording site of a waking-specific neuron marked with pontamine sky blue in the ventral TM.b, A waking-specific neuron stained with both Nb and HA (arrows and arrowhead).c, A non-waking-specific neuron labeled only with Nb (arrowhead).b,c, Arrows indicate neurons stained only with HA. The arrow ina shows the recording site of a waking-specific neuron in the ventral tuberomammillary nucleus marked with pontamine sky blue.
Figure 3.
Figure 3.
A,B, Spike shape of waking-specific (A) and waking-active (B) neurons. Note that waking-specific neurons are characterized by a broad triphasic action potential, whereas waking-active and other TM neurons are characterized by a biphasic (either narrow or broad) action potential. The arrowheads inA1 andA2 indicate the positive deflection. InA3 andB3,D1–D4 indicate the duration of the averaged action potential measured from onset (t0) to the peak (D1), the first zero crossing (D2), the peak of the afterhyperpolarization (D3), and the second zero crossing (D4), shown inA1.
Figure 4.
Figure 4.
Activity of a representative waking-specific neuron. Note that activity is confined to waking periods, with the cell being completely silent during sleep. Note also the absence of discharge during short awakening periods (arrowheads) during sleep. The large arrow indicates the end of PS, as shown by the interruption of theta waves and the onset of EEG desynchronization. The small arrows with an “s” indicate short awakenings elicited by the arousing sound stimulus.
Figure 5.
Figure 5.
Activity of a representative waking-specific neuron during the different waking states.
Figure 6.
Figure 6.
A,B, Activity of a representative waking-active neuron (A) and discharge profile of waking-active (B1) and waking-specific (B2) neurons across the sleep–waking cycle.
Figure 7.
Figure 7.
A,B, Discharge pattern of a waking-specific neuron during behavioral state transitions (A) and response to an arousing sound stimulus (B). InA, the transition from SWS to W is shown as t1, that from W to drowsy state is shown as t2, and that from PS to W is shown as t3. Note that the unit fires with a long delay after the onset of EEG desynchronization of W, whereas it stops firing during quiet waking before the onset of the drowsy state, defined by EEG synchronization. Note also that there is no, or a long-delayed, response to a sound stimulus given during sleep.
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