Elsevier

Autonomic Neuroscience

Volume 99, Issue 1, 31 July 2002, Pages 24-30
Autonomic Neuroscience

Firing patterns of micturition-related neurons in the pontine storage centre in cats

https://doi.org/10.1016/S1566-0702(02)00055-3Get rights and content

Abstract

The pontine storage centre (PSC) and the pontine micturition centre (PMC) are known to be critical for urinary filling and emptying, respectively. In the present study, firing patterns of 45 neurons in the PSC area where electrical stimulation induced inhibition of the micturition reflex were analyzed in 20 male decerebrated and paralyzed cats. The electrically determined PSC area was widespread in the dorsolateral pontine reticular formation (P0–P4), ventrolateral to the PMC. Four major types of neurons were detected according to urinary storage/micturition cycles: tonic storage neurons (38%), phasic storage neurons (40%), tonic micturition neurons (9%) and phasic micturition neurons (13%). These four types of neurons were intermingled in the PSC. However, the tonic and phasic micturition neurons tended to be located within a limited area (P2–P3). These neurons were further classified into augmenting, constant and decrementing firing patterns. Some increased their firing prior to the storage/micturition phase initiation. Such preceding pattern was more frequently found in the tonic neurons than in the phasic neurons. In conclusion, the PSC neurons with diverse heterogeneous discharge patterns suggest that these neurons may organize a complex neuronal circuitry, which is critical in the neural control of the urinary continence.

Introduction

Previous anatomical and physiological studies have revealed that the micturition reflex is dependent on neural circuitry in the pons de Groat et al., 1993, Blok and Holstege, 1999. Two major structures involved in the micturition reflex exist in the area. One is known as the pontine micturition centre (PMC) (de Groat et al., 1993), Barrington's nucleus Barrington, 1921, Barrington, 1925, Valentino et al., 1999 or M region Holstege et al., 1986, Blok and Holstege, 1999, which is located in or adjacent to the locus coeruleus in cats, dogs, possibly in humans Betts et al., 1992, de Groat et al., 1993, Nishizawa and Sugaya, 1994, Sakakibara et al., 1996, Blok et al., 1997, Valentino et al., 1999, Blok and Holstege, 2000 and in the laterodorsal tegmental nucleus in rats (Satoh et al., 1978a, Satoh et al., 1978b; to et al., 1989). Lesions in the PMC result in severe urinary dysfunction such as urinary retention in experimental animals de Groat et al., 1993, Blok and Holstege, 1999 as well as in humans Betts et al., 1992, Sakakibara et al., 1996. Electrical or chemical stimulation of the PMC initiates micturition reflex Noto et al., 1989, Mallory et al., 1989, Mallory et al., 1991, Griffiths et al., 1990 by activating a descending pathway to the sacral parasympathetic preganglionic nucleus, which innervates the urinary bladder muscles Holstege and Kuypers, 1982, Valentino et al., 1999, Blok and Holstege, 2000. The other area is known as the pontine storage centre (PSC) Nishizawa et al., 1987, de Groat et al., 1993, or L region Holstege et al., 1986, Blok and Holstege, 1999, which is located ventrolateral to the PMC. Bilateral lesions in the PSC give rise to an inability to store urine; bladder capacity is reduced and urine is expelled prematurely by excessive detrusor activity accompanied by urethral relaxation (Blok and Holstege, 1996). The PSC activation terminates or inhibits the micturition reflex together with an excitation of the pelvic floor musculature Griffiths et al., 1990, Blok and Holstege, 1999 including the urethral sphincter innervated by the sacral Onuf's nucleus Holstege and Tan, 1987, Blok et al., 1998. Neurophysiological studies have demonstrated that the PMC neurons discharge with several firing patterns, including neurons that fire predominantly during micturition and predominantly during urinary storage Bradley and Conway, 1966, Okada and Yamane, 1974, de Groat et al., 1998. In contrast, neuronal activities in the PSC have yet to be investigated. Thus, this study aimed to examine discharge patterns of the PSC neurons that may be crucial for the urinary continence.

Section snippets

Experimental preparation

Experiments were done on 20 adult male cats (3.2–4.0 kg) that were decerebrated at the precollicular level. Surgical preparation was performed under anesthesia with halothane vaporized in nitrous oxide and oxygen. The trachea was intubated and catheters were placed in the femoral artery to monitor blood pressure and in the femoral veins for drug administration. A double-lumen urinary catheter was inserted into the bladder transurethrally to measure bladder pressure and to regulate bladder

Results

The location of the PMC and PSC was identified by the responses of bladder contractions to electrical stimulation. The typical responses of bladder pressure to PMC and PSC stimulation are seen in Fig. 1Aa and Ab, respectively. The PMC was located within a relatively limited area in the vicinity of the locus coeruleus (Fig. 1B). In contrast, the PSC was distributed in a broader area, mainly ventrolateral to the PMC, extended rostrocaudally (P0–P4) overlapping to the dorsolateral pontine

Discussion

The location of the PSC has been investigated in both anatomical and physiological manners. Morphological studies have revealed that the sacral Onuf's nucleus, which innervates the urethral sphincter, receives a direct projection from a discrete area located ventrolateral to the PMC, named the L region Holstege and Kuypers, 1982, Holstege et al., 1986, Holstege and Tan, 1987. On the other hand, the detrusor relaxation and the external sphincter contraction are elicited by electrical stimulation

Conclusions

The existence of a variety of heterogeneous discharge patterns observed in the PSC neurons suggest that these neurons may organize a complex neuronal circuitry, which is critical in the neural control of the urinary continence and the micturition/storage phase initiation.

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