Select spinal lesions reveal multiple ascending pathways in the rat conveying input from the male genitalia

Abstract

The specific white matter location of all the spinal pathways conveying penile input to the rostral medulla is not known. Our previous studies using rats demonstrated the loss of low but not high threshold penile inputs to medullary reticular formation (MRF) neurons after acute and chronic dorsal column (DC) lesions of the T8 spinal cord and loss of all penile inputs after lesioning the dorsal three-fifths of the cord. In the present study, select T8 lesions were made and terminal electrophysiological recordings were performed 45-60 days later in a limited portion of the nucleus reticularis gigantocellularis (Gi) and Gi pars alpha. Lesions included subtotal dorsal hemisections that spared only the lateral half of the dorsal portion of the lateral funiculus on one side, dorsal and over-dorsal hemisections, and subtotal transections that spared predominantly just the ventromedial white matter. Electrophysiological data for 448 single unit recordings obtained from 32 urethane-anaesthetized rats, when analysed in groups based upon histological lesion reconstructions, revealed (1) ascending bilateral projections in the dorsal, dorsolateral and ventrolateral white matter of the spinal cord conveying information from the male external genitalia to MRF, and (2) ascending bilateral projections in the ventrolateral white matter conveying information from the pelvic visceral organs (bladder, descending colon, urethra) to MRF. Multiple spinal pathways from the penis to the MRF may correspond to different functions, including those processing affective/pleasure/motivational, nociception, and mating-specific (such as for erection and ejaculation) inputs.

Figure 1. Effect of sub-total dorsal hemisection (DHx)

Example showing the location of pelvic nerve (PN)-responsive MRF neurons in 3 rats with a chronic sub-total dorsal hemisection lesion (DHx) at T8 (bottom panel) compared to the location of neurons described in Hubscher & Johnson (2004) for spinally intact animals (top panel, n= 3) and animals with a bilateral dorsal column lesion (DCx) at T8 (middle panel, n= 3). All of these neurons also responded to bilateral electrical stimulation of the dorsal nerve of the penis (DNP). Responses to low (stroke) and high (pinch) threshold levels of mechanical stimulation of the penis are listed for each group. Note a lack of responses to stroke following DCx but a re-emergence following extension of the lesion to the medial portions of the DLF bilaterally and sparing the lateral DLF on one side. Inserts illustrate the extent of the lesion (X). Cross section is adapted from Fig. 65 of Paxinos & Watson (1998).

Figure 2. MRF single unit recording

Example of convergent inputs to a PN-responsive single neuron located in left nucleus reticularis gigantocellularis at 60 days post-injury. Epochs are 6 and 12 s. An image taken from the chronic lesion epicentre for this rat is provided. The central canal, which can be seen in the middle of the section, orients both the dorsal/ventral and medial/lateral extents of the lesion. Note the presence of the responses to stroking the penis. The horizontal bar symbols on the raw records indicate the onset and duration of the hand-held stimulus application. The arrows (and the stimulus artifacts) indicate the onset of an electrical stimulus train to the respective nerve (stimulus train duration 100 ms, 70 pulses at 0.2 ms pulse duration).

Figure 3. VLF lesion effects

Examples of lesion epicenter reconstructions from three male rats illustrating the location of ascending pathways in the ventral half of the spinal cord to MRF from the glans penis, pelvic nerve (PN) and other input territories (bladder, urethra, descending colon). The presence of a few responses to penile stimulation in the rat whose lesion is shown in the centre panel is likely to be due to some lateral sparing on the left side of the spinal cord. Likewise, the presence of some responses to pinching the hind paw (left foot only) in the rat whose lesion is shown in the right panel is likely to be due to some medial ventrolateral funiculus sparing on the right side of the spinal cord. Hatch marks indicate overlap of white matter areas (illustrated on just one side) whose damage results in the loss of penile (middle panel) and pelvic nerve (right panel) ascending projections. Note that to completely eliminate all responses to these somatovisceral convergent neurons in the MRF, the lesion must be bilateral. HT – high threshold, L – left, LT – low threshold, R – right.

Figure 4. Ascending penile projections to MRF

A summary diagram illustrating the approximate locations of multiple bilateral ascending pathways at the mid-thoracic spinal level conveying sensory information from the glans penis to the medullary reticular formation (MRF). The different stimulus thresholds to trigger a neuronal response in MRF are indicated. HT – high threshold; LT – low threshold.