Anatomical Evidence for Interconnections Between the Central Mesencephalic Reticular Formation and Cervical Spinal Cord in the Cat and Macaque

Abstract

A gaze-related region in the caudal midbrain tegementum, termed the central mesencephalic reticular formation (cMRF), has been designated on electrophysiological grounds in monkeys. In macaques, the cMRF correlates with an area in which reticulotectal neurons overlap with tectoreticular terminals. We examined whether a region with the same anatomical characteristics exists in cats by injecting biotinylated dextran amine into their superior colliculi. These injections showed that a cat cMRF is present. Not only do labeled tectoreticular axons overlap the distribution of labeled reticulotectal neurons, these elements also show numerous close boutonal associations, suggestive of synaptic contact. Thus, the presence of a cMRF that supplies gaze-related feedback to the superior colliculus may be a common vertebrate feature. We then investigated whether cMRF connections indicate a role in the head movement component of gaze changes. Cervical spinal cord injections in both the cat and monkey retrogradely labeled neurons in the ipsilateral, medial cMRF. In addition, they provided evidence for a spinoreticular projection that terminates in this same portion of the cMRF, and in some cases contributes boutons that are closely associated with reticulospinal neurons. Injection of the physiologically defined, macaque cMRF demonstrated that this spinoreticular projection originates in the cervical ventral horn, indicating it may provide the cMRF with an efference copy signal. Thus, the cat and monkey cMRFs have a subregion that is reciprocally connected with the ipsilateral spinal cord. This pattern suggests the Abbreviations used: BC 5 brachium conjunctivum; cMRF 5 central mesencephalic reticular formation; Cun 5 cuneiform nucleus; C1 5 first segment of the cervical spinal cord; C2 5 second segment of the cervical spinal cord; C3 5 third segment of the cervical spinal cord; DF 5 dorsal funiculus; DH 5 dorsal horn; DR 5 dorsal raphe; EWu 5 urocortin containing; Edinger Westphal nucleus; IC 5 inferior colliculus; InC 5 interstitial nucleus of Cajal; LF 5 lateral funiculus; MG 5 medial geniculate nucleus; MRF 5 midbrain reticular formation; nB 5 nucleus of the brachium of the inferior colliculus; nPC 5 nucleus of the posterior commissure; PAG 5 periaqueductal gray; piMRF 5 peri InC mesencephalic reticular formation; PRF 5 pontine reticular formation; Pt 5 pretectum; SN 5 substantia nigra; R 5 red nucleus; SC 5 superior colliculus; SGI 5 intermediate gray layer; SGP 5 deep gray layer; SOA 5 supraoculomotor area; Vc 5 spinal trigeminal nucleus pars caudalis; VF 5 ventral funiculus; VH 5 ventral horn; 3 5 oculomotor nucleus; 4 5 trochlear nucleus.

A central mesencephalic reticular formation projection to the supraoculomotor area in macaque monkeys

“…Reticulospinal neurons projecting to cervical spinal cord and medullary reticuloreticular cMRF neurons projecting to the rostral medullary reticular formation occupy just the medial portion of the cMRF (Fig. 11A) [primate: (Castiglioni et al 1978; Perkins et al 2014; Robinson et al 1994; Warren et al 2008); cat: (Perkins et al 2014; Satoda et al 2002)]. As we have shown here, the presence of a narrow band of cells labeled from oculomotor injections, reveals an unreported subdivision with direct projections to the SOA and III (Fig.…”

“…Further examination of the feedback pathway revealed that the ipsilateral reticulotectal projection was GABAergic, and the contralateral projection contained both GABAergic and non-GABAergic elements (Wang et al 2010). The role of the cMRF in controlling head movements also was supported by anatomical studies in cats and monkeys (Perkins et al 2009; Warren et al 2008; Zhou et al 2008). Specifically, cMRF projections to the cervical cord and to reticulospinal neurons in the medullary reticular formation were demonstrated.…”

“…After 10–30 minutes of preincubation, hydrogen peroxide was added to produce a 0.005 % solution. WGA-HRP was revealed by utilizing tetramethylbenzidine as a chromagen (Olucha et al 1985; Warren et al 2008). Following these reactions, sections were rinsed in PB, mounted, counterstained with cresyl violet, dehydrated, cleared and cover slipped.…”

Projections from the brain to the spinal cord in the mouse

“…The red nucleus sends a major tract to the contralateral spinal cord in mammalian and non-mammalian vertebrates (Kuypers et al 1962;Poirier and Bouvier 1966;Warner and Watson 1972;Miller and Strominger 1973;Castiglioni et al 1978;Crutcher et al 1978;Wild et al 1979;Smeets and Timerick 1981;Huisman et al 1982;Carlton et al 1985;Okado and Oppenheim 1985;Prasada Rao et al 1987;Nudo and Masterton 1988;Masino and Knudsen 1992;New et al 1998;Cruce et al 1999;Carretta et al 2001;Satoda et al 2002;Tsukamoto et al 2003;Chiocchetti et al 2006;VanderHorst and Ulfhake 2006;Stockx et al 2007;Warren et al 2008). As with the corticospinal projection (see above), the exception is the hedgehog, in which the ipsilateral projection is larger than the contralateral (Kunzle 1992).…”

Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation

“…One possibility is that stimulation recruited fibers that traverse through the PPRF region and relay projections to the neck motoneurons (e.g., May and Porter 1992;Warren et al 2008). Another candidate is a subset of reticulospinal neurons that reside in the PPRF region Robinson et al 1994).…”